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Frontispiece. — The Anderson Tree Frog, Hyla andersonii, calling with
inflated vocal pouch. Flashlight study.

THE BIOLOGY OF
THE AMPHIBIA

G. KINGSLEY NOBLE, Ph.D.

Curator of Herpetology and Experimental Biology, The American
Museum of Natural History

PRIVATE LIBRARY OF
ALBERT G« SMITH

McGRAW-HILL BOOK COMPANY, Inc.

NEW YORK AND LONDON
1931

First Edition

PRINTED IN THE UNITED STATES OF AMERICA

All rights reserved. This book, or
parts thereof, may not be reproduced
in any form without permission of
the publishers.

THE MAPLE PRESS COMPANY, YORK, PA.

PREFACE

With the increasing use of both frogs and salamanders in
experimental biology, the need has arisen for a general textbook
which summarizes the relations of Amphibia to one another and
to their environments. The salamanders, for example, are
commonly believed to be more primitive than frogs, although
this is true for only certain features of their anatomy. Again,
Necturus, which is now frequently employed in university courses
of zoology, is often described as a very primitive type, without
further reference to its systematic position among the Caudata.
There is no book written in English since Gadow's volume in the
" Cambridge Natural History" (1901) which attempts to combine
both the natural history and the biology of Amphibia in a single
volume. Holmes's splendid book on "The Biology of the Frog"
has accomplished this task for Rana, and in extending the field
to all the Amphibia, I have been influenced by this work in the
selection of material.

Although the present volume was written primarily to intro-
duce the student to the biology of both frogs and salamanders,
technicalities have been avoided wherever possible and much
has been included which should be of interest to the field natural-
ist or traveler. The systematic names employed are those in
current use by naturalists and not the more familiar ones of the
experimental laboratory. The difference between these two
nomenclatures is not sufficiently great, however, to cause
confusion.

The sections dealing with the physiology of Amphibia are
necessarily greatly abridged, but reference has been made
wherever possible to the more comprehensive papers and sum-
maries where a historical treatment of the subject may be found.
Unfortunately, the extensive account of the Amphibia by Pro-
fessor Franz Werner in Kukenthal's "Handbuch der Zoologie"
appeared after my manuscript had gone to press and no reference
is made to this authoritative work in the following pages.

In the preparation of the text I have received help from many
sources. My thanks are due first to Professor Henry Fairfield

vii

viii

PREFACE

Osborn for his enthusiastic interest and for the many facilities
I have enjoyed at the American Museum where the work was
carried forward. I have received considerable bibliographical
assistance from Dr. Cora S. Winkin and Mr. Ludwig Hirning,
who have also collated various parts of the text. Dr. Winkin
has contributed original notes to the chapters dealing with the
nervous system and with metabolism. Professor Frank H.
Pike has kindly read the chapters on the nervous system and on
respiration. Dr. Thomas Barbour has loaned for study valuable
material preserved in the Museum of Comparative Zoology.
The drawings are the work of Mrs. E. L. Beutenmuller and many
are based on original material in the American Museum. I am
especially appreciative of the aid given throughout the course of
the work by my research assistant, Miss Gertrude Evans.

G. K. N.

The American Museum of Natural History
New York, N. Y.,
April, 1931.

ACKNOWLEDGMENTS

Many of the figures used in the text have previously appeared
in my papers published in the Bulletin and in Novitates of the
American Museum as well as in the Annals of the New York
Academy of Science. I am indebted to the authorities of the
Museum and to the Academy for the privilege of republishing
them. Many others have been taken from various scientific
journals and books and I wish to express my obligation to the
publishers and the authors for the opportunity of redrawing these
figures for the present work. Acknowledgment of this courtesy
is made to the following sources:

Academie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique

for Fig. 68 from Bull. Acad. Roy. Belg. CI. Sci.
Akademische Verlagsgesellschaft, for Fig. 100 from Zool. Anz., Figs.

65, 92, 92D from Morph. Jahrb., Figs. 118, 119 from Zeitschr. Wiss. Zool.
American Microscopical Society for Figs. 103 A, 1035, 114B, 138 from

Trans. Amer. Micr. Soc, Figs. 78A, 78B, 115 from Proc. Amer. Micr.

Soc.

Bergmann-Verlagsbuchhandlung, J. F., for Figs. 117, 122 from Anat. Hefte.
Bonnier, Albert, for Fig. 114A from Acta Zoologica.

Cambridge University Press and The Macmillan Company for Fig. 130
from Coghill, "Anatomy and the Problem of Behaviour."

Crowell Company, Thomas Y., for Fig. 126 from Papez, "Comparative
Neurology."

Deutsche geologische Gesellschaft for Fig. SB from Zeitschr. Deutsch. Geol.
Gesellschaft.

Essex Institute, The, for Fig. 82 from Bull. Essex Inst.

Fisher, Gustav, for Figs. 60, 64, 72 from Anat. Anz., Figs. 65, 6C
from Biol. Unters., Fig. 97 from Hertwig's "Handbuch der
vergleichenden und experimentellen Entwickelungslehre der Wirbel-
tiere," Fig. 125 from Jena. Zeitschr. Naturw. Fig. 9 from Kernel's
"Normentafeln zur Entwicklungsgeschichte der Wirbeltiere," Fig. 128C
from Kuhlenbeck " Vorlesungen uber das Zentralnervensystem der
Wirbeltiere," Fig. 123 from Zool. Jahrb., Abt. Allg. Zool. Physiol.
Tiere, Figs. Ill, 128A, 129 from Zool. Jahrb., Abt. Anat.

Folia Anatomica Japonica, Editors of the, for Figs. 84A, 84B, 84C, 842?,
128B from Folia Anat. Japonica.

Hokkaido Imperial University for Fig. 133 from Jour. College Agr.

Hollandsche Maatschappij der Wetenschappen and F. J. J. Buytendyk for
Fig. 134 from Arch. Neerland. de Physiol, de I'Homme et des Animaux.

Marine Biological Laboratory for Figs. 7 A, 52, 103C from Biol. Bull.

ACKNOWLEDGMENTS

New York Zoological Society for Fig. 133F from Zool. Soc. Bull.

Royal Society, The, for Figs. 1, 2, 83 from Phil. Trans. Roy. Soc. London,

Figs. 56 A, 565 from Proc. Roy. Soc. London.
Smithsonian Institution for Figs. 77, 139 from U. S. Nat. Mus. Bull.
Springer, Julius, for Figs. 3A, 10 from "Ergebnisse naturwissenschaftlicher

Forschungen auf Ceylon" (Sarasins), Figs. 13, 55 from Arch. Mikr.

Anat., Fig. 8 from Zeitschr. Zell. Gewebel.
Taylor and Francis for Figs. 4, 85 from Ann. Mag. Nat. Hist.
Thieme, Georg, for Figs. 79, 106, 132 from Biol. Zentralbl.
University of California Press for Fig. 137 from Univ. Calif. Pub. Zool.
University of Chicago Press for Fig. 16 from Physiol. Zool.
University of Wisconsin for Fig. 71 from Bull. Univ. Wis.
University Press Cambridge for Figs. 12, 112 from Brit. Jour. Exp. Biol.
Wegner, Julius E. G., for Fig. 133D from Bldtt. Aquar.-Terrar.-Kde.
Wistar Institute of Anatomy and Biology for Fig. 109 from Anat. Rec,

Fig. 108 from Amer. Anat. Mem., Figs. 69, 70, 75 from Amer. Jour.

Anat. Figs. 113, 116, 120, 124, 127 from Jour. Comp. Neurol, Figs.

15, 101, 107 from Jour. Exp. Zool, Figs. 6D, 10A, 14, 93, 98, 102, 105,

121 from Jour. Morph.
Zoological Society of London and Dr. O. M. B. Bulman for Fig. 5 from Proc.

Zool Soc.

CONTENTS

Page

Preface vii

Acknowledgments ix

PART I

THEIR STRUCTURE AND FUNCTIONS

Chapter

I. The Origin of the Amphibia

The First Tetrapods — Piscine Ancestors — Labyrinthodontia —
Phyllospondyli — Lepospondyli— Modern Amphibia.

II. Development and Heredity 15

Fertilization — Cleavage — Gastrulation — Larvae — M echanics
of Development — Epigenesis — Basis of Homology — Develop-
ment of Limbs — Influence of Function — Regeneration — Rela-
tion of Regeneration to Development — Regenerative Capacity
— Hybridization.

III. The Mode of Life History 48

Cryptobranchidae — Proteidae — Ambystomidae — Salamandri-
dae — Amphiumidae — Plethodontidae — Terrestrial Plethodon-

t i ds — Salientia — Brevicipitidae — Ranidae — Poly pedatidae —
Hylidae — Brachycephalidae — Bufonidae — Ovoviviparous Bu-
fonids — Primitive Salientia — Gymnophiona — The Primitive
Type.

IV. Speciation and Adaptation 79

Species Denned — Variation — Hereditary Units — Isolation in
Species Formation — Kinds of Isolation — Space and Time in
Evolution — Natural Selection — Divergent Evolution — Parallel
Evolution — Function in Phylogeny — Adaptation — Preadapta-
tion— Physiological Characters — Hormones in Evolution —
Permanent Larvae — The Course of Phylogeny.

V. Sex and Secondary Sex Characters 108

Functional Significance of Secondary Sex Characters — Unex-
plained Sexual Differences — Phylogeny of Secondary Sex
Characters — Relation of Secondary Sexual to Somatic Charac-
ters— Discontinuous Evolution.

VI. The Integument 130

Unicellular Glands — Comparison with Fish — Poison Glands —
Other Glands — Odors — Horny Growths — Molt — Skin as a

xii

CONTENTS

Chapter

Page

Respiratory Organ — Pigmentation — Color Change — Color Pat-
terns— Influence of the Environment on Pigmentation —
Significance of Color.

VII. The Respiratory System

158

Gills — Relation of Gill Form to Function — Integument in
Respiration — Lungs — Larynx — Ways of Respiration — Lung-
lessness — Comparison with other Vertebrates — Respiratory
Responses.

VIII. The Circulatory System

179

Blood Corpuscles — Phagocytosis — Origin of Blood Corpuscles
— Blood Vessels — Heart — Modifications of the Heart — Func-
tion of the Heart — Lymphatic System.

IX. The Digestive System

201

Stomach — Intestines — Glandular Outgrowths — Digestion —
Absorption and Assimilation — Modifications of Digestive
Tract.

X. The Skeleton

212

Skull — Progressive Modification of the Skull — Modification of
the Palate — Changes in the Jaws — Auditory Apparatus — Vis-
ceral Skeleton — Laryngeal Skeleton — Vertebrae — Ribs — Ab-
dominal Ribs — Pectoral Girdle — Pelvic Girdle — Limbs — Skele-
ton of Modern Amphibia.

XI. The Muscular System 247

Body Muscles — Modification of Body Muscles — Ventral
Throat Musculature — Forelimb Muscles — Comparison of Frog
and Salamander — Hind Limb Musculature — Visceral Muscles.

XII. The Urogenital System 266

Urogenital Organs — Function of the Kidney — Reproductive
System — Urinary Bladder — Sex and Its Modification — Seg-
mentation of the Gonads — Fat Bodies — Ovulation — Fertiliza-
tion— Structure of the Cloaca — Evolution of the Spermatheca
— Identification of Sex.

XIII. The Endocrine Glands 290

Thyroid Gland — Thyroid and Metamorphosis — Iodine and
Metamorphosis — Pituitary Gland — Pars Anterior — Pars Inter-
media— Pars Posterior — Pancreas — Adrenal Organs — Gonads

— Parathyroids and Ultimobranchial Body — Thymus — Pineal
Organ.

XIV. The Sense Organs and Their Functions 317

Lateral-line Organs — Tactile Organs — Organs of Chemical
Sense — Heat and Cold Receptors— Organs of Taste — Olfactory
Organs — Eyes — Accommodation — Retina — Degeneration of
the Eye— Ears — Inner Ear — Functions of the Ear — Other
Internal Mechanoreceptors — Dominant Senses — Smell, Taste,
and Common Chemical Sense — Hearing — Vision and Sensi-
tivity to Light — Rheotropism — Thigmotaxis — Responses to
Internal Stimulation.

CONTENTS xiii

Chapter Page

XV. . The Nervous System 353

Reflex Arc — Brain — Forebrain — Thalamus — Midbrain Roof —
Cerebellum — Medulla — Phylogeny of the Brain — Spinal Cord
and Nerves — Autonomic System.

XVI. Instinct and Intelligence 377

Development of Reflexes in Ambystoma — Multiple Uses of
Single Reflexes and Instincts — Defense Reaction — Phylo-
genetic Change of Instincts — Mechanism of Instinct — Learned
Behavior — Intelligence.

XVII. The Ways of Amphibia 399

Migration — Direction of Migration — Homing — Voice — Signifi-
cance of Voice — Recognition of Sex — Parental Instinct — Feed-
ing Habits — Responses to Temperature Change — Temperature
Preferences — Responses to Humidity Change— Defense —
Tonic Immobility — Leaping of Salamanders and Frogs.

XVIII. The Relation of Amphibia to Their Environment .... 431
Metabolism of Amphibia — Temperature and Behavior —
Metabolism and Behavior — Fuel of Metabolism — Hormones
and Metabolism — Effect of the Environment — Microscopic
Parasites — Larger Parasites — Other Enemies — Length of Life.

XIX. Geographic Distribution and Economic Value 448

Geographical Distribution — Land Bridges — Age and Area —
Barriers to Dispersal — Economic Value.

PART II

RELATIONSHIPS AND CLASSIFICATION

Order 1. Labyrinthodontia 459

Order 2. Phyllospondyli 461

Order 3. Lepospondyli 462

Order 4. Gymnophiona 463

Order 5. Caudata 465

Order 6. Salientia 485

Index 545

THE BIOLOGY OF THE
AMPHIBIA

PART I

THEIR STRUCTURE AND FUNCTIONS

CHAPTER I
THE ORIGIN OF THE AMPHIBIA

There are many backboned animals which lead an amphibious
life. The crocodile and the seals live at times in water and
again on land. The name " Amphibia," first used by Linnaeus for
a rather odd assemblage of more or less aquatic vertebrates,
referred to this amphibious habit of the members of the group.
Today the name is restricted to that class of vertebrates which is
intermediate between fishes and reptiles. The group includes the
frogs, salamanders, caecilians, and many fossil creatures, fre-
quently of large size and bizarre form.

The living Amphibia are cold-blooded vertebrates possessing
limbs instead of paired fins like the fish and having a soft, moist
skin lacking the protective hair or feathers of higher vertebrates.
Salamanders are often confused with lizards, which they resemble
superficially. The latter have a dry, scaly skin similar to that
of other reptiles. Minute scales are present between the trans-
verse body rings of caecilians but these are rarely seen without
making a dissection. Amphibia may, therefore, be defined as
cold-blooded vertebrates having a smooth or rough skin rich in
glands which keep it moist; if scales are present, they are hidden
in the skin.

The development of Amphibia, also, serves to distinguish them
from reptiles, birds, or mammals. The eggs are usually laid in
the water and the larvae pass through an aquatic stage before
metamorphosing into the adult. Many frogs and salamanders
lay large-yolked eggs on land and the young never enter the
water. These terrestrial eggs lack the calcareous shell of reptiles

THE BIOLOGY OF THE AMPHIBIA

and birds. Further, the embryo as it develops is never sur-
rounded by the protective amnion or equipped with a respiratory
allantois as in the case of higher vertebrates. Modern Amphibia
differ from reptiles in many details of their skeletal anatomy,
but some Carboniferous and Permian Amphibia, especially the
Rachitomi, were so similar to contemporary reptiles that it is
impossible to draw a sharp line of distinction between them.
Palaeontological discoveries have also done much to fill in the
gap between Amphibia and fishes but even here all the inter-
mediate stages have not yet "been found. Modern Amphibia
have arisen from a group of more or less aquatic tetrapods which
flourished from at least early Carboniferous to Triassic times.

The term "Batrachia" is frequently used for the class
Amphibia, as, for example, by Cope in his monumental "The
Batrachia of North America." Linnaeus included crocodiles,
lizards, snakes, and turtles in his group Amphibia, and he was
followed by some later students. Brongniart was the first to
distinguish the frogs and salamanders from the reptiles but his
choice of the term batraciens for the group was unfortunate, as
this name was already a synonym of Salientia. Various other
names were later proposed for the class. It was not until 1825
that Latreille restricted the name Amphibia to the frogs, toads,
and salamanders, leaving the caecilians with the reptiles. The
term Amphibia, therefore, originates from the Linnaean name
as restricted by Latreille, the caecilians being later added to
the group. Rules of priority are not strictly applied to groups
higher than genera, and as Linnaeus included reptiles in his
category, there are some students who would use another name
for the class. Since none of the later names proposed has met
with wide acceptance, the majority of recent students utilize the
Linnaean name Amphibia in its restricted sense. (Noble, 1929.)

The First Tetrapods. — If we compare a frog sitting on the
edge of a pond with the perches, catfish, or eels in the water, the
difference between a tetrapod and a fish seems tremendous. A
scrutiny of their detailed structure brings forth such a series of
differences in skull, appendages, and breathing apparatus that
the change from fish to frog would seem to be one of the most
radical steps in the evolution of the vertebrates.

This step does not seem less tremendous when we compare the
aquatic newt with the fish, for the former is a typical tetrapod
which has secondarily taken up a life in the water. It is no

THE ORIGIN OF THE AMPHIBIA

wonder that anatomists were puzzled for many years as to how
the first tetrapod arose, and even today there is no agreement
between those who study only the recent forms.

When the evidence from palaeontology is available, this must
necessarily be placed ahead of all our other evidences. The
gaps in the palaeontological record of the Amphibia are great,
but the combined researches of recent years (especially Gregory,
1915; Watson, 1917, 1919, 1926; Williston, 1925) have thrown
much light on the beginnings of land life among the vertebrates.
Further, most amphibians pass their early life in the water.
The morphological changes of metamorphosis would seem to
reflect to a greater or lesser extent the changes which took place
when the first vertebrate became established on land. As with
all other problems of phylogeny, the evidence of palaeontology,
of anatomy, and of development must be weighed one against
the other for the final solution of the problem.

If the modern fish were to be changed into a tetrapod, a number
of important transformations of structure would have to be
accomplished. The gills would have to be lost, and the lungs
developed and the nasal passage extended to form internal nares
for the ingress of air when the mouth is closed. The fins and
body would have to be modified for land locomotion and the
integument changed to resist drying. The latter would mean
the development of a cornified epidermal covering and a series
of integumentary glands discharging by ducts on to the surface,
at least over those parts not provided with an armored skin.
Specialized glands would be required to keep the nasal passage
and mouth from drying. The eyes, formerly bathed by the
water, would be especially sensitive to the new conditions and
must either develop a horny, protective cover as in modern
snakes or produce softer eyelids out of dermal folds. In either
case a lacrimal gland and drain would be needed for cleansing
the eyeball. To keep the nasal passage clean a muscular closing
device would be required at the outer end of each nasal inlet.
If the first tetrapod were to succeed on land, the sense organs of
the fish would have to undergo considerable modification, for,
while the lateral-line organs would be no longer required, the
auditory, optic, and olfactory centers would gain a higher
importance, demanding in some cases fundamental changes in
the structure of the organs. If the head were flat as that of
many frogs, special muscles to raise the eyes above the surface

THE BIOLOGY OF THE AMPHIBIA

of the skull would be needed if the eyes were to be at all efficient.
Lastly, the loosely hung jaw of the majority of teleosts would
have to be firmly fixed to the brain case.

How the first tetrapod accomplished all these changes will
never be known. The evidence available shows conclusively
that it was not by such sudden revolution as maintains in the
metamorphosis of most modern forms. The outstanding contri-
bution of the palaeontological data is the proof of how slight a
structural alteration changed the primitive fish ancestor into
the first land vertebrates. Similarly, the first reptiles evolved
from the embolomerous amphibians and the first mammals from
cynodont reptiles by very gradual steps.

Piscine Ancestors. — Today there are a few fish which live
both in and out of water. Some of these have been recently
carefully studied by Harms (1929) and it is interesting to note
how closely they parallel the Amphibia in their adaptations to
life on land. Protection against drying is secured by the develop-
ment of a horny skin growth in the gobies and a cuticle in the
blennies. Skin respiration is improved by the penetration of
capillaries into the epidermis. An extensive saccular enlarge-
ment of the buccopharyngeal cavity increases the efficiency of
buccal respiration. Gulped air is prevented from escaping
through the gill slits by a modification of the gill covers. The
eyes are modified to project above the surface of the head, and
the limbs, especially the posterior, are strengthened by bony
rays so arranged as to permit terrestrial locomotion. There are
also changes in the cutaneous sense organs which protect them
against drying. These fish undergo a certain metamorphosis
into partly terrestrial animals, and Harms found that this
metamorphosis was influenced by the thyroid hormone, as in
the case of Amphibia.

The first tetrapods did not come from modern fish. Already
in Carboniferous times three distinct orders of tetrapods —
labyrinthodonts, lepospondyls, and phyllospondyls — had devel-
oped. The first two were both present in the Lower
Carboniferous. Footprints are known from the Devonian of
Pennsylvania. Hence the tetrapods must have arisen in at
least Devonian and possibly Silurian times. The tetrapods
arose from ancestors in the fresh waters, for their earliest remains
are associated with fresh-water deposits. All fresh-water fishes
of Devonian times were ganoids (in the broad sense), dipnoans, or

THE ORIGIN OF THE AMPHIBIA

aberrant sharks, and hence our search for the tetrapod ancestor
narrows down to these lines of primitive fishes.

If we compare the modern dipnoans and ganoids with modern
Amphibia, especially urodeles, certain obvious resemblances will
at once appear. Both breathe to a large extent by lungs and
the distributions of blood vessels to and from these organs have a
close resemblance. Other similarities may be found in certain
features of the skull (Wintrebert, 1922), the brain (Herrick, 1924),
the urogenital system, and early development. But these
similarities will not bear a close inspection, for they differ in
many details.

It is, however, hardly reasonable to compare a modern amphib-
ian with a modern dipnoan when the ancestral stocks of both
groups are available for study as fossils. The most primitive
dipnoans, those from the Middle Devonian, may have possessed
some of the urodele resemblances listed above, but they also
possessed a number of distinctive characters which would
preclude them from the direct ancestorship of modern Amphibia.
This is especially true of the skull which had already begun the
formation of the large tooth-plates so characteristic of modern
lung fishes. In many other features of their skull the primitive
dipnoans differ widely from their tetrapod contemporaries.

This leaves only the ganoids among which to find the ancestor
of all tetrapods, since the sharks are obviously off the main line
of ascent. One family of Devonian crossopterygian ganoids, the
Osteolepidae, agree so closely with the primitive Amphibia in
most important skeletal features that there can be no doubt that
the first tetrapods branched off from a fish very closely allied
to this family. The work of Dollo, Watson, Gill, etc., has made
it clear that the dipnoans and the osteolepids sprang from the
same stock. Whether the Amphibia sprang from this ancestral
stock or from the very base of the crossopterygian stem is not
known. They agree in structure more closely with the Oste-
olepidae than with the earliest fossil dipnoans. In seeking the
beginnings of tetrapod organization in the fishes, our attention
must, therefore, be turned not to modern dipnoans nor to
crossopterygians, nor to the fossil dipnoans, but to the osteolepid
crossopterygians of Devonian times which differed but slightly
from the actual ancestors of the Amphibia.

The most primitive Amphibia are the Embolomeri, an extinct
suborder which lived from Lower Carboniferous to the Permian

THE BIOLOGY OF THE AMPHIBIA

(Fig. 1). Our knowledge of the skeletal details of the Embo-
lomeri are chiefly due to the brilliant researches of Watson (1926).
The Embolomeri, like many later groups of Amphibia, very
early underwent an enormous adaptive radiation. Already in
Carboniferous times the group contained, as shown by Watson
(1926, page 192), " primitively aquatic animals which show no
signs of ever having possessed terrestrial ancestors/ ' others
obviously terrestrial, and still others secondarily returned to
life in the water. " Despite these diverse habits, the funda-

Fig. 1. — Eogyrinus attheyi, a primitive embolomerous amphibian. Recon-
struction of the skeleton. {After Watson, Phil. Trans. Roy. Soc. London, 1926.)

mental morphology of the skeleton is strikingly uniform through-
out the group.' ' The ancestral fish, as shown by Watson,
changed into a tetrapod before the latter became permanently
adapted to land life.

Labyrinthodontia. — The earliest Amphibia as represented by
Eogyrinus, recently made known by Watson (1926), swam in
the waters with their piscine ancestors. Amphibia were pre-
pared for life on land before they were forced into the terrestrial
world. Still it is probable that a need for terrestrial adaptations
existed at the time the Amphibia were evolving. Eogyrinus
apparently lived in pools of a rather arid and quickly drying
country. With the drying of the pools Eogyrinus would have
been forced to make overland journeys to new pools. Loco-
motion over land was probably made very much in the manner
of an eel.

The first Amphibia were essentially fishlike in most of their
skeletal anatomy. In the osteolepid fishes a long tract of the
basis cranii remained unossified permitting a certain movement
of the skull, while in the embolomerous Amphibia this had
ossified (Fig. 2). The fish hyomandibular was converted into a
stapes in the earliest Amphibia even though no opening for its
insertion into the otic capsule was present. A true stapes in
these Embolomeri suggests that a tympanic membrane was
present covering the spiracular notch. As in fish, the pectoral

THE ORIGIN OF THE AMPHIBIA

girdle of some Embolomeri was attached to the skull by the post-
temporal bones and closely resembled that of fish except that a
new dermal element, the interclavicle, had been added to its
ventral surface in the midline. The pelvis of these early Embolo-
meri gave evidence that the first Amphibia were not primarily

Fig. 2. — Skull of an osteolepid fish and an embolomerous amphibian compared.
Side view: A. Osteolepis macrolepidotus . B. Palaeogyrinus decorus. Palate view:
C. Baphetes. D. Eusthenopteron. B.Oc, basioccipital; B.Sp., basisphenoid ;
Ec.Pt., ectopterygoid; E.Pt., epipterygoid ; Ju., jugal; L., lacrimal; Mx., maxilla;
Pal., palatine; P.Mx., premaxilla; P.O., postorbital; Pr., prefrontal; Pr.Ot., pro-
otic; Pt., pterygoid; P.V., prevomer; Qu.J., quadratojugal; Sq., squamosal.
(After Watson, Phil. Trans. Roy. Soc. London, 1926.)

terrestrial. The long sacral ribs lay below an elongated ilium,
indicating that the latter element was attached to them by
muscles, exactly as the scapula is attached to the pectoral ribs.
The limbs were small but as far as known more like those of
later Amphibia than like the fins of the osteolepoid fishes. Fin-
gers and toes were present and the limbs assumed a normal

THE BIOLOGY OF THE AMPHIBIA

position at right angles to the axis of the body. The limbs of the
Embolomeri perhaps more than any other part of the skeleton
show an advance over the homologous structures of fish.

The Embolomeri are grouped with other crocodile- or sala-
mander-like Amphibia in the order Labyrinthodontia. These
have a skull with a solid covering of many more bones than are
found in the skull roof of modern Amphibia. Only the eyes,
nostrils, pineal foramen, and rarely the facial pit, formed openings

in this solid skull cover. The teeth
were pointed with simple or greatly
folded dentine layers. It is from these
folded teeth that the order receives its
name. Frequently bony plates or scales
were present in the skin, forming a
protection for the ventral surfaces
which were dragged over the ground,
also a cover delaying the desiccation of
the body and in some instances a
cuirass against the attacks of enemies
(Fig. 3).

The evolution of the Labyrinthodontia
is essentially a process of reduction of
ossification. This results in an increase
in the interpterygoid vacuities of the
skull, the change of the joint between
skull and first vertebra from a single or
tripartite condyle to a double condyle,
and the modification of the vertebrae
from a double centrum to a single cen-
trum type. These changes in the skele-
sins). B. Several scales of ton are considered in further detail in

Discosaurus, a labyrintho-

Fig. 3. — Comparison of
the scales of a modern and
an extinct amphibian. A.
A single scale of Ichthyophis,
a caecilian {after the Sara

dont (after Credner).

Chap. X, while a classification of the
order is given in the concluding chapter.
The suborders Embolomeri, Rachitomi, and Stereospondyli
represent successive grades in the evolution of skull and vertebrae.
The vertebrae evolved away from the reptile type for the inter-
centrum (basiventral) was emphasized in the Stereospondyli
at the expense of the pleurocentrum which tends to disappear
(or remain cartilaginous). In modern Amphibia this reduc-
tion is carried even further; an ossification in the connective
tissue sheath surrounding the chorda forms the greater part

THE ORIGIN OF THE AMPHIBIA

of the centrum, although the basidorsal and usually the
basiventral are represented by cartilages. The pleurocentrum
(interdorsal and interventral) may remain unossified, forming
the cartilaginous joint between the successive vertebrae, or the
greater part may ossify as the "ball" of the centrum. If this
ball attaches itself to the vertebra anterior to it, the vertebra is
procoelous; if to the one behind, it is opisthocoelous.

Phyllospondyli. — Contemporaneous with the Embolomeri there
occurred in both Europe and America a group of small Amphibia
which were apparently destined to give
rise to the frogs and salamanders at a
later period. These were the Phyllos-
pondyli (Fig. 4) as represented by Eugy-
rinus in Lancashire, England, and Pelion
in the Pennsylvanian of Linton, Ohio
(Romer, 1930). Pelion retained such
primitive features as an ectopterygoid,
as well as an articulation of the pterygoid
with the anterior margin of the basi-
sphenoid region much as in the Embolo-
meri. Large labyrinthodont teeth were
present medial to the row of marginal
teeth. Romer considers this form ances-
tral to the typical branchiosaurs in which
the labyrinthodont teeth were greatly
reduced or lost and the pterygoid had a
more posterior position and was presum-
ably firmly fixed to the cranium. Typical
branchiosaurs as represented in the late
Pennsylvanian horizon of Bohemia had short, broad skulls, still
retaining the tabulars and the dermosupraoccipitals, lost by all
modern Amphibia (Fig. 5) . The ribs were short and straight as in
frogs and salamanders and were carried by transverse processes
from the side of the vertebrae. Primitive frogsagree so closely with
salamanders in vertebrae and skull that it would seem certain they
had a common origin. The branchiosaurs resembled salamanders
closely in body form. No fossils have been found with skull or
pectoral girdle intermediate between that of branchiosaurs and
urodeles. Nevertheless the ribs, limbs, pelvis, and vertebrae of
branchiosaurs resemble those of urodeles so much that it seems
highly probable that salamanders and also frogs arose from the

Fig. 4. — Restoration of
Branchiosaurus flagrifer.
{After Whittard.)

THE BIOLOGY OF THE AMPHIBIA

branchiosaurs. At least there is no group of fossil Amphibia
which they resemble more fully.

In the coal measure deposits there are found a variety of other
small Amphibia which cannot be grouped with the Labyrintho-
dontia. Some of these in the Linton formation, such as Colosteus
and Stegops, may be considered aberrant branchiosaurs (Romer,
1930). It is interesting that the latter should have " horns"
projecting from the posterior angles of its skull. In frogs a
similar horn development occurs in certain genera but here
involving other bones. Stegops also exhibits dentigerous
plates in the roof of the mouth underlying the eye sockets.

A B

Fig. 5. — Reconstruction of the skull of Leptorophus tenet, a branchiosaur
amphibian. A. Dorsal surface. B. Palate view. D.S.O., dermosupraoccipital;
F.P., postfrontal; Ju., jugal; L., lacrimal; Mx., maxilla; Na., nasal; Pa., palatine;
P.F., prefrontal; Pmx., premaxilla; P.O., postorbital; P.V., prevomer ; Proc.Pal.,
Processus palatinus of maxilla; Psp., parasphenoid ; Pt., pterygoid; Q.J., quad-
ratojugal; Qu., quadrate; Sq., squamosal; Tab., tabular. (After Bulman and
Whittard.)

A similar development of crushing plates occurs in certain
species of the salamander, Desmognathus. Other parallels
may be drawn between vertebrae, limbs, and various other
features of these Phyllospondyli with similar structures in either
frogs or salamanders.

Lepospondyli. — In the same deposits as the Phyllospondyli
and Labyrinthodontia there occurs a variety of other amphibian
types which may be grouped together in another order, Lepos-
pondyli, although they seem to have little in common. The
vertebrae are usually formed of a single piece without sutures,

THE ORIGIN OF THE AMPHIBIA

the centrum being hourglass shaped, and the ribs are generally
intercentral in position. There are, however, exceptions to
both these rules. The Adelospondyli, considered by Watson
(1926a) a distinct order, has the neural arch joined by suture
with the centrum which is cylindrical in shape and indented by a
deep pit on either side. The transverse process is anterior in
position and the rib is thus nearly intervertebral in position.
The centrum is solid except for a small notochordal foramen
and is not the thin shell found typically in branchiosaurs. The
group is represented in America by Cocytinus of the Pennsylvan-
ian and Lysorophus of the Permo-Carboniferous. If this group
arose from the Embolomeri it must have split off in Devonian
times. The best-known genus is Lysorophus (Sollas, 1920).
In many characters of the skull it resembles the caecilians closely.
Limbs and a well-ossified branchial apparatus were present,
however. Lysorophus has been described as a Permian "uro-
dele," but its principal urodele characters, other than those just
mentioned, are found also in caecilians. The structure of its
vertebrae and skull excludes it from the order Caudata.

Legless Amphibia were present in the Carboniferous but these
resemble caecilians in neither skull nor vertebrae. These were
the Aistopoda which may be considered a suborder of Lepo-
spondyli. They differ from typical lepospondyls in their large
transverse processes and distinctive ribs.

One of the most bizarre groups of lepospondyls is the Nectridia
which specialized in the development of a "horn" on either angle
of the head. In the last of the line in America, Diplocaulus of
the Permo-Carboniferous, the head had the form of a Colonial
cocked hat. Diplocaulus, as shown by Douthitt (1917), retained
various reptilian features such as a separate coracoid and possibly
a fifth finger. The primitive Nectridia had a skull structure
resembling the embolomerous plan and hence it seems probable
that the group arose at the time the Embolomeri were evolving
on one hand into reptiles and on the other into higher labyrintho-
donts. Well-developed transverse processes are present on the
vertebrae of the Nectridia, a parallel to the Phyllospondyli.
These Nectridia were too specialized in skull structure to be
considered ancestral to any modern Amphibia. While various
lepospondyls approach the urodeles in the structure of their
vertebrae they possess other characters which exclude them from
the direct line of ancestry. On the other hand, the caecilians,

THE BIOLOGY OF THE AMPHIBIA

which are more primitive than any other modern Amphibia in
many details of their anatomy, may have directly evolved from
lepospondyls. If this is true, caecilians had an independent
line of evolution from Lower Carboniferous or Devonian times.
The many differences between the structure of caecilians and
that of other modern Amphibia would support such a view.

Modern Amphibia. — The three orders of Amphibia living
today may be distinguished at a glance from one another. The
Salientia, or frogs and toads, have short, tailless bodies in adult
life and long hind legs, the latter being effective organs for leap-
ing. The Caudata, or salamanders and newts, retain the larval
tail throughout life and have short legs of use in walking but not
in rapid flight. The Gymnophiona, or caecilians, are wormlike,
burrowing creatures of the tropics with a very short tail usually
resembling the head in form and without any indication of limbs.
All three orders differ radically from the extinct orders of Amphibia
in having lost many skeletal elements. The suppression of
bones in the orbital series makes possible a proportionately larger
eye in modern forms. The loss of the dermal bones along the
posterior margin of the skull gives them a more compact skull.
Both temporal and back muscles tend to cover the otic region
even in the most primitive of the modern Amphibia and the
temporal bones of the extinct groups are either lost or greatly
modified in modern forms. There are also marked differences
in other parts of the skeleton; these will be considered in further
detail below. Modern Amphibia are frequently considered more
primitive than reptiles which are supposed to form the next
" higher" class of vertebrates. The primitive reptiles grade
imperceptibly into the Embolomeri and many living reptiles
retain primitive structures which have been lost in all modern
Amphibia. The reptile skull, with its more complete skull roof
and its twelve cranial nerves, is more primitive than that of
modern Amphibia. The shoulder girdle of many reptiles,
especially that of lizards with a well-developed interclavicle, is
more primitive than the girdle of modern Amphibia. The highly
glandular skin, the development of cutaneous respiration, the
loss of the external ear in many species represent deviations from
the primitive conditions which were not shared by most reptiles.

Nevertheless, all reptiles have advanced beyond the first
tetrapods in the direction of birds and mammals in their manner
of protecting the eggs against desiccation and of embryonic

THE ORIGIN OF THE AMPHIBIA

modifications for respiration and storing of waste products.
The labyrinthodonts passed through an aquatic larval stage
in the water as shown by the retention of the larval respiratory
apparatus in certain forms such as Dwinasaurus. This indirect
method of development was handed on to the branchiosaurs
and to modern Amphibia. Reptiles, at a very early stage in
their evolution, succeeded in producing a leathery or calcareous
cover to their egg. Further, the growing embryo forced into
the large yolk produced a cover for itself, the amnion, by folding
over the extra-embryonic tissue immediately surrounding it.
The embryo removed from the surface of the egg next succeeded
in producing a saclike diverticulum of the cloacal region, the
allantois, which served both for respiration and for storing
solid wastes of metabolism. Although many modern Amphibia
lay eggs on land and some embryos are partially forced into the
yolk as they develop, no amphibian has succeeded in making
these important changes in egg and growing embryo which were
so important for the future evolution of land vertebrates. An
aquatic larval life is not characteristic of all Amphibia, but none
develops from eggs with calcareous shells, and none produces an
amnion or allantois.

Modern Amphibia are mostly small creatures. The giant
salamander, Megalobatrachus, reaches a length of over 5 feet,
the Goliath Frog may reach a length of nearly a foot in head and
body length, but most salamanders and frogs are not over a foot
in total length.

References

Douthitt, H., 1917: The structure and relationships of Diplocaulus,
Contrib. Walker Museum, II, No. I, 3-41.

Gregory, W. K., 1915: Present status of the problem of the origin of the
Tetrapoda, with special reference to the skull and paired limbs, Ann.
N. Y. Acad. Set., XXVI, 317-383.

Harms, J. W., 1929: Die Realisation von Genen und die consecutive Adap-
tion; I, Phasen in der Differenzierung der Anlagenkomplexe und die
Frage der Landtierwerdung, Zeitschr. Wiss. Zool, CXXXIII, 211-397,
5 pis.

Herrick, C. Judson, 1924: "Neurological Foundations of Animal Behav-
ior," New York.

Noble, G. K., 1929: Amphibia "Encyclopaedia Brittannica," 14th ed., I,
832-840.

Romek, A. S., 1930: The Pennsylvanian Tetrapods of Linton, Ohio, Bull
Amer. Man. Nat. Hist., LIX, 77-147.

THE BIOLOGY OF THE AMPHIBIA

Sollas, W. J., 1920: On the structure of Lysorophus as exposed by serial

sections, Phil. Trans. Roy. Soc. London, Ser. B, CCIX, 481-527.
Watson, D. M. S., 1917: A sketch classification of the Pre-Jurassic tetrapod

vertebrates, Proc. Zool. Soc. London, 1917, 167-186.
, 1919: The structure, evolution and origin of the Amphibia — the

"orders" Rachitomi and Stereospondyli, Phil. Trans. Roy. Soc. London,

Ser. B, 1920, CCIX, 1-73.
, 1926: The evolution and origin of the Amphibia, Phil. Trans.

Roy. Soc. London, Ser. B, CCXIV, 189-257.
, 1926a: The Carboniferous Amphibia of Scotland, Palaeontologica

Hungarica, I, 221-252, 3 pis.
Williston, S. W., 1925: "Osteology of the Reptiles," Harvard Univ. Press,

Cambridge.

Wintrebert, P., 1922: L'Evolution de Fappareil pterygo-palatin chez
les Salamandridae, Bull. Soc. Zool. France, XLVII, 208-215.

CHAPTER II

DEVELOPMENT AND HEREDITY

The egg of frog or salamander, when freshly laid, is a single
cell. If fertilized, it develops by a series of orderly changes
into a complex organism, an adult amphibian. The processes of
development and heredity are so closely interwoven that they are
conveniently considered together.

Development begins with the fertilization of the eggs or ova.
These are produced by the ovary and they have a long growth
period before they are released from that organ. The sper-
matozoa are formed in the testes and represent single cells
greatly elongated and modified for locomotion. The sper-
matozoa of Salientia exhibit a great variety of form according to
the species, while those of the urodeles are singularly uniform
(Fig. 6). The acrosome or point of the urodele spermatozoon
is frequently bent like the barb on a fishhook. The head is
lance-shaped and formed by the transformation of the nuclear
matter of the male germ cell. Before this transformation takes
place the number of chromosomes in each germ cell is reduced
by half by a division which gives half the number of whole
chromosomes to the daughter cells, instead of the whole number
of chromosomes, divided longitudinally in half, as in ordinary
cell division. The middle piece and tail of the spermatozoa are
formed from the cytoplasm or from structures in the cytoplasm
of the germ cells.

Fertilization. — The eggs of most frogs are fertilized externally
and usually by the male who is embracing the female when the
eggs are laid. The egg capsules absorb water rapidly after
laying and soon can be no longer penetrated by the sperm.
The ovoviviparous frogs of Africa, Nectophrynoides, practice
internal fertilization, although no external organs for trans-
fering the sperm are known in these frogs. In the " tailed"
frog of America, Ascaphus, the "tail," an extension of the
cloaca, serves as an intromittent organ. External fertiliza-
tion characterizes the two most primitive families of urodeles,

THE BIOLOGY OF THE AMPHIBIA

Fig. 6. — Spermatozoa of various
amphibians. A. Desmognathus phoca.
B. Bombina bombina (after Retzius). C.
Hyla arborea (after Retzius). D. Crypto-
branchus alleganiensis (after Smith).
Cy.B., cytoplasmic body.

Hynobiidae and Crypto-
branchidae, but all higher
groups except the specialized
Meantes possess a series of
tubules in the roof of the
female cloaca which retain,
for varying periods, the sper-
matozoa usually picked up en
masse in the form of a sper-
matophore (Fig. 7) by the
female with her cloacal lips.
These tubules known collec-
tively as the " spermatheca "
are homologous with a smaller
or greater part of the pelvic
gland of the male (Noble and
Pope, 1929). It has been
assumed that the eggs are
fertilized as they pass by the
spermatheca, but there is
evidence that in Salamandra
at least, the spermatozoa
migrate up the oviduct before
the time of egg laying
(Weber, 1922).

The spermatozoa make
their way through the gelat-
inous capsules of the egg,
aided by the swimming move-
ments of their tails and
apparently also by the diges-
tive action they exert on the
capsules (Wintrebert, 1929).
In the case of the primitive
frog, Discoglossus, the sper-
matozoa, although more than
2 mm. in length, are almost
completely immobile (Hib-
bard, 1928). Nevertheless,
they are carried through a
thickened portion of the egg

DEVELOPMENT AND HEREDITY

capsules overlying a depression in the surface of the egg
by their digestive powers. Why the spermatozoa accumulate
only in the region of this depression has not been determined.
Miss Hibbard suggests that the nuclear fluids which collect
at the bottom of the depression may exert a chemotactic effect
on the sperm. In the common frog, Rana, although a much
higher type than Discoglossus, there is less localization of the
area of penetration. The first spermatozoon to reach the darker
hemisphere of the egg sets up a fertilization reaction. After it

Fig. 7. — Spermatophores of common salamanders. A. Triturus viridescens
(after Smith). B. Desmognathus fuscus (after Noble and Weber). C. Eurycea
bislineata.

has entered the egg, the latter forms a fertilization membrane
which prevents the entrance of other spermatozoa. In Caudata
several spermatozoa normally enter the egg but only one sperm
nucleus combines with the egg nucleus, the others degenerating
before segmentation is far advanced. The number of sper-
matozoa which may safely enter the urodele egg, without causing
irregularities of development leading to death, stands roughly
in proportion to the size of the egg. Polyspermy obtains among
eggs, such as those of Cryptobranchus, in which the mass of yolk
is considerable. It seems to be a device for large eggs, insuring
that one sperm at least shall enter at a point near the egg nucleus.
Fertilization includes two processes: activation or the removal
of the block to development, and syngamy or the union of the
nucleus of the egg with that of the spermatozoon. The first
process may be induced artificially in frogs by pricking the egg

THE BIOLOGY OF THE AMPHIBIA

with a needle (Bataillon, 1910). The second process makes
possible the transmission of hereditary factors received from the
male and may be considered in more detail.

Eggs extracted from the ovaries of the frog before they have
escaped into the body cavity cannot be fertilized. This seems
due to the failure of such eggs to maturate. In this process two
successive divisions of the egg result in the throwing off near
the animal pole of two minute bodies which are actual daughter
cells although very small and difficult to see. One of these
divisions results in relegating to the small functionless daughter-
cells half of the chromosomes. Hence the egg nucleus at the

Fig. 8. — Stages in the spermatogenesis of Rana temporaria. A. Metaphase of
a spermatogonial division showing the 26 chromosomes characteristic of this
species. B. Second maturation division showing the x and y chromosomes
(in outline) between the autosomes. C. Immature spermatozoon. (After
Witschi.)

moment of fertilization has only half the chromosome number
found in the body cells (Fig. 8). The union with the male nucleus
(which by a similar pair of divisions has reduced its chromosome
number by half) results in the restoration of the original somatic
number of chromosomes. This number is constant for the
species, ranging from 32 for Alytes to 12 for Pelodytes. Several
frogs and salamanders have a somatic number of 24. In Rana
pipiens, R. palustris, and R. sylvatica there are 26 chromosomes;
in several species of Bufo only 22 (Stohler, 1928).

The spermatozoon brings to the egg little besides this nuclear
matter. The acrosome or point (Fig. 6) is formed by the trans-
formation of certain cytoplasmic materials, the product of the
Golgi bodies, and may possibly represent a secretory granule

DEVELOPMENT AND HEREDITY

which sets off the fertilization reaction (Bowen, 1924) or at least
digests the egg capsules. The middle piece, or neck, is derived
from other cytoplasmic material and carries one or two bodies,
the centrioles, one of which forms a center of cell division
after the sperm enters the egg. In urodeles the neck is
better marked than in Salientia and formed of only a single
centriole. The tail, which is long and vibratory, is left outside
when the spermatozoon enters the egg. There is at present no
definite evidence that any of these cytoplasmic materials play
any part in heredity. The hereditary factors of the male parent
are brought in by the sperm nucleus while those of the female
are located in the nucleus of the egg. It is known from the com-
bined researches of genetics and cytology that the chromosomes,
the most conspicuous part of the nuclei, are the bearers of genes,
the determiners of heritable characters. The genes lie in a
linear order along the chromosomes. Their ultimate nature is
still unknown but they have been compared with protein bodies
and have been assumed to release enzymes which take part
in the catalytic reactions in the cytoplasm of the cell.

The chromosome complex is handed on by cell division to all
the cells of the body. Since the cells of the skin have the same
number of chromosomes (except in certain unusual cases) as
the fertilized egg, the question arises: What has determined that
they will become skin instead of remaining germ cells? What,
in brief, produces differentiation?

The frog's egg, even before fertilization, has a certain organiza-
tion which affects the pattern of differentiation. It has an
apicobasal polarity, as shown externally by the distribution of
the pigment. The pigmented pole has less specific gravity than
the yolk-laden vegetative pole and hence floats uppermost. This
is made possible by the extrusion from the egg of a fluid which
collects under the vitelline membrane, facilitating the rotation
of the egg within the capsules. During development the egg
rotates further and this apicobasal axis becomes the longitudinal
axis of the tadpole. The other two axes are established at the
moment of fertilization. A gray crescent, caused by the retreat
of the pigment from the surface opposite the point of penetration
of the spermatozoon, gives the egg bilaterality, and as this
crescent is on the future dorsal side, the dorsoventral axis is
indicated. Pricked frogs' eggs have gray crescents without
relation to the point of pricking (Herlant, 1911). Hence eggs

THE BIOLOGY OF THE AMPHIBIA

Fig. 9. — The development of Necturus maculosus. A. Side view of egg 1
day and 8 hours after deposition, showing second and third cleavage grooves.
B. Bottom view of egg 6 days and 16 hours old. The crescentic blastopore lip
sharply separates the large-yolk cells from the small cells of the blastodisc. C.
Bottom view of egg 10 days and 10 hours old, showing large circular
blastopore. D. Top view of egg 14 days and 4 hours old. Blastopore smaller.
The beginning of neural fold formation, especially anteriorly. E. Top view of
egg 15 days and 15 hours old. Yolk plug still visible. Neural fold prominent.
Its free ends reach nearly to the blastopore. F. Top view of egg 18 days and 15
hours old with three or four pairs of myotomes visible. G. Dorsolateral view of
embryo 22 days and 17 hours old; length 8 mm.; 16 to 18 myotomes. H. Side

DEVELOPMENT AND HEREDITY

probably have an initial bilaterality of their own which is over-
ridden by the stimulus introduced by the spermatozoon.

Cleavage. — The fertilized egg divides into many cells (Fig. 9).
As the egg increases only slightly in size during the period of
cleavage, the nuclear material is brought into close relationship
with smaller units of cytoplasm. At every division nuclear
material is liberated into the cytoplasm; enzymes or other
substances released by the genes are thus brought in close associa-
tion with the cytoplasm. The cleavage pattern has little phylo-
genetic significance. All amphibian eggs are comparatively
soft and cleavage is total. If the yolk of the frog's egg is packed
down by centrifuging, cleavage may be partial as in higher
vertebrates without detriment to the embryo (Hertwig, 1899).
The eggs of Amphibia vary enormously in the amount of yolk
they contain and there is considerable evidence that the simplified
cleavage pattern found in the common frog has been secondarily
imposed by a reduction in the amount of yolk in the egg. The
cleavage of Hemidactylium is more diagrammatic than that of
Eurycea, for although a more specialized type, its eggs contain
less yolk (Humphrey, 1928). A cleavage which is diagrammatic
is not necessarily primitive in any vertebrate. Cleavage is a
period of rearrangement of nuclear material in relation to the
cytoplasm. Qualitative changes do not occur, hence alteration
of cleavage pattern by pressure has no permanent effect on the
embryo. Cleavage results in the formation of a hollow sphere
with walls usually several cells thick. The hollow or blastocoel
is frequently very shallow and in the large-yolked species may be
merely a slit between apical cells and underlying yolk.

Gastrulation. — A certain amount of differentiation occurs
before cleavage. This is revealed externally by the formation
of the gray crescent alluded to above. If this region is cut
away from the egg the latter is unable to develop (Moszkowski,
1902). In the urodeles, a gray crescent has been described in
the axolotl (Vogt, 1926) but it is scarcely visible in the European
newts which have been extensively studied by Spemann and his
associates. During cleavage the cells of the pigmented hemi-
sphere of the egg divide more rapidly than the heavily yolk-
view of embryo 26 days old; length 11 mm.; 26 to 27 myotomes; eye, ear, nasal
pits, and mouth well defined. /. Side view of embryo 36 days and 16 hours old;
length 16 mm.; 36 to 38 myotomes. Side view of larva 49 days old; length 21
mm. K. Side view of larva 97 days old; length 34 mm. {After Eycleshymer and
Wilson.)

THE BIOLOGY OF THE AMPHIBIA

laden cells of the opposite pole. A continuation of this process
causes the cells of the first region to tend to grow over those of
the second. The gray crescent region takes the lead in cell
proliferation and becomes the dorsal lip of the blastopore, growing
as a crescentic fold over a section approximately 100 degrees of
the egg. The slitlike cavity between lip and infolded yolk
cells represents the archenteron, or rudiment of the gut. This
eventually either opens at its anterior end into the blast ocoel
or obliterates it by crowding. Since the overgrowth of the cells
of the dorsal hemisphere extends completely around the egg, the
blastopore becomes a gradually diminishing circular fold engulfing

Fig. 10. — Blastopore of a salamander and caecilian compared. In salamanders
and most frogs the overgrowth of cells of the dorsal hemisphere during gastrula-
tion extends completely around the egg; in caecilians the blastodisc or overgrowth
forms a circular blastopore while the yolk hemisphere is still uncovered. A.
Late blastopore of Cryptobranchus {after Smith). B and C. Two stages in the
formation of the blastopore of Ichthyophis {after the Sarasins). B.D., blastodisc;
B.P., blastopore; N.PL, neural plate.

the more slowly dividing yolk cells. In some plethodontid
salamanders, the circle remains incomplete ventrally and the
blastopore takes the form of an inverted crescent (Humphrey,
1928). The embryo-forming materials of the gray crescent
are at first broadly distributed as a ring or crescent about the
circumference of the egg. They are brought together not only
by overgrowth during gastrulation but also by concrescence
of the two halves of the gray crescent in the midline. Hence
the point of concrescence, namely the dorsal lip of the blastopore,
comes to have a more important role in organ formation than
the ventral lip.

In frogs and salamanders the whole of the yolk hemisphere is
covered over as the blastopore closes, but it is a very interesting
fact that in the caecilians, which seem to have descended inde-
pendently from primitive tetrapods, the blastopore becomes
circular while the yolk hemisphere is still largely uncovered
(Fig. 10). In this way the blastopore becomes surrounded by

DEVELOPMENT AND HEREDITY

blastodisc while the latter still remains on the upper surface of a
partly divided egg. This is a very important step in the direc-
tion of reptilian development. If the developing embryo should
sink into this blastodisc until the surrounding tissue folded over
it as an amnion, if cleavage were further delayed in the yolk
hemisphere, and if, as development proceeded, the urinary
bladder were converted into a large respiratory membrane, the
allantois, the gap between amphibian and reptilian types of
development would be bridged. The earliest Amphibia, as
revealed by their fossil skeletons, were hardly separable from
the earliest reptiles. It seems likely that their mode of develop-
ment resembled that of the caecilians, many of which today lay
their eggs on land. In any case, the result of gastrulation is
the development of a double-layered sac out of a single-layered
hollow sphere, and this event is of great significance in the origin
of structures.

Larvae. — The frog embryo, as it develops within the egg capsule,
shows various conformations which can be identified as the anlage
of organs. The head end exhibits two swellings which may be
recognized as eyes. Between them, and sometimes extending
posteriorly in the midline, is a more densely pigmented stripe.
This is the site of the unicellular hatching glands (Chap. VI)
which are destined to free the larvae of both frogs and salamanders
from their egg capsules. A conspicuous pit in the developing
head of the frog embryo may be recognized as the mouth. At
this early stage the deepest part of the pit in some species of
Rana is formed by the hypophysial ingrowth of the pituitary
(Chap. XIII). The position of the future external nares is
indicated by a pair of depressions, above and usually lateral
to the mouth. Below the mouth a pair of pigmented eminences,
or frequently a V-shaped furrow, is the first indication of the
growing adhesive organs (Fig. 11). At the time of hatching
these structures form a pair of adhesive organs of value in per-
mitting the larva to hold to its egg capsule, or other objects.
In most salamander larvae these adhesive organs find their
homology in a pair of glandular stalks, the balancers, which
project from near the angle of the mouth and have the same func-
tion as the adhesive organs of tadpoles. These structures are
further discussed in the following chapter.

Immediately caudal to the optic eminences a series of three
or four ridges indicates the developing branchial arches of both

THE BIOLOGY OF THE AMPHIBIA

frog and salamander larvae. The external branchiae early
begin to sprout on these arches as a number of small buds. With
development a fold appears anterior to the first of these gills.
In the frog tadpole this is destined to grow back over the external
gills and form an opercular sac which remains in communication
with the exterior by one or two small openings, the spiracles.
An opercular fold is represented in salamander larvae but it

Fig. 11. — The head structures of the early larva of a toad, Gastrophryne
carolinensis. The adhesive organs function at the time of hatching to hold the
tadpole to objects in the water. The oro-nasal groove forms the beginning of the
nasal chamber. Ad.Org., adhesive organ; N.Pit., nasal pit; O.N.Gr., oro-nasal
groove; St., stomodaeum.

never completely covers the branchial arches until the time of
metamorphosis.

The chief difference between the larvae of frogs and sala-
manders lies in the mouth region. In most frog tadpoles, lips
are formed and these acquire a series of horny teeth arranged
in rows above and below a pair of strong mandibles. These
nippers are supported internally by a pair of cartilages, called
" superior" and " inferior labial cartilages." The former, which
articulate with cartilaginous processes of the brain case, are
destined to form the premaxillaries of the adult; the latter,
the mento-Meckelian bones. The inferior labial cartilages are
supported by a pair of short cartilages, the very rudimentary
Meckelian, or lower jaw cartilages. Most remarkable is the

O.N.

Gr.

.Ad Org.

DEVELOPMENT AND HEREDITY

forward extension of the palatoquadrate cartilage of each
side to give support to these Meckelian cartilages. In sala-
manders, horny teeth or typical mandibles never appear, and
the jaws which are well provided with true teeth are long from
the first stages of development. This apparently enormous
difference in the structure of the mouths of tadpole and sala-
mander is bridged over by various intermediate types. As stated
below (page 52), some salamanders have horny plates on their
jaws, and many frog tadpoles, as, for example, most Brevicipi-
tidae, lack horny teeth.

Some of the developing internal organs are indicated on the
outer surface of the embryos or larvae of frogs and salamanders.
Of these, the most conspicuous is the pronephros. The develop-
mental history of these structures is given in the following chap-
ters, and only the external changes of development need be
indicated here. The adhesive organs and balancers are lost at
about the time the larvae begin to feed. The gills elongate
and in salamanders assume a form more or less characteristic
of the species. In frogs the extent of the operculum and the
position of its spiracle differ with the species. The vent, which
becomes perforated at this time, may lie on the side of the tail
fin or ventral to it, and this position is again a character of sys-
tematic importance. The intestine in most frog tadpoles becomes
very long and coiled like a watch spring. As discussed in a
following chapter, this is an adaptation to the vegetarian diet
of most tadpoles and is not characteristic of all species. In
frog tadpoles the forelimbs develop within the opercular sac
and do not appear until the time of metamorphosis. The hind
limbs of both frog and salamander continue their growth during
larval life. The lungs are present in the larvae of most frogs
and salamanders and function both as hydrostatic and respiratory
structures. At the end of larval life the frog tadpoles lose their
larval teeth, tail, and gills. The eyes develop lids, and many
pronounced changes of skull and viscera occur. Metamorphosis
in salamander larvae is less revolutionary, for a broad mouth and
true teeth are already present. Nevertheless, many changes
occur in the skull, skin, and respiratory system. These changes
are discussed in detail below (Chaps. VI, VII, and X).

Mechanics of Development. — The tissues which take part
in the formation of the. various structures of Amphibia are being
analyzed experimentally by an increasingly large number of

26 THE BIOLOGY OF THE AMPHIBIA

investigators. Some of their more general conclusions may be
considered here, for they have an important bearing on the causes
of the diversity of structure distinguishing species. At the close
of gastrulation the potencies for organ formation are segregated
in various parts of the embryo, although there may be no external
evidence of this mosaic formation of qualitatively unlike regions.
Little or no regulation can occur if one of these regions is removed.
Thus, if an area destined to produce a forelimb is dissected
away from an Amby stoma embryo at the time of the appearance

remain permanently limbless
(Harrison, 1915). In con-
sidering the origin of struc-
ture one must examine first
the origin of potencies.

At the very beginning of
gastrulation the embryo of
the newt is not a mosaic
of potential parts. If a piece
of ectoderm which would be-
come neural plate is trans-
planted into the place which
would become gills, it develops
into gills. A little later in
gastrulation the same opera-
tion will produce no change,
for the presumptive neural
plate tissue remains neural
plate. If the exchange is
made at the beginning of
gastrulation between the em-
bryos of two species of newts
readily distinguished by their color, the tissue which would
have become neural plate is molded into gill tissue as before,
but the tissue resembles that of the donor species in color and
character. During gastrulation, transplanted tissue may be
molded by the host embryo (Figs. 12, 13) but this tissue does
not lose its specific identity (Spemann, 1928).

What is the nature of this molding influence? Spemann
and his associates have shown that it emanates from the turned-in
dorsal lip of the blastopore, the gray crescent region of the frog's
egg. Geinitz (1925) transplanted a piece of this potential

of the tail bud, the region will

A B

Fig. 12. — The effect of an organizer.
A. Neurula of the newt, Triturus taeni-
atus, with a secondary medullary plate
(the narrow white band) induced by a
transplanted organizer from another
species of newt, T xristatus. B.
Embryo of T.taeniatus seen from the
left side. The secondary embryonic
growth consists of neural tube and
some associated structures. (Both after
Spemann.)

DEVELOPMENT AND HEREDITY

chorda-mesoderm into the archenteron of a European newt
and found that it induced the overlying ectoderm to form a
neural plate. Since the secondarily induced embryo need not
have the same orientation as the primary one, the organizer has a
longitudinal axis of its own. Further, it has some laterality,
for if dorsal lip tissue from one side is replaced by tissue from the
opposite side of another egg, two similar half embryos tend to
develop from the egg. Nevertheless, the molding influence, or

Fig. 13. — Section of an egg of the newt, T. taeniatus, in which a piece of dorsal
lip from the egg of T.cristatus has been transplanted and has induced there a
secondary embryo. L.Sec.Lab., left secondary ear vesicle; Pc, pericardium;
Pr.Med., primary medullary tube; Sec. Med., secondary medullary tube. (After
Spemann and Mangold.)

" organizer," as it is called, is nothing specific. Geinitz (1925)
showed that gray crescent material from a frog, Bombina, could
induce a secondary embryo in a newt. The organizer seems to
be something retained in the tissues for a considerable time.
A neural tube induced by a piece of dorsal lip tissue when trans-
planted into the archenteron of a young gastrula induces another
neural tube to form in the overlying ectoderm. Mangold and
Spemann (1927) have shown that brain tissue from a free-swim-
ming tadpole can induce the formation of a medullary plate.
This makes it appear likely that the organizer is chemical in
nature. Nevertheless, the organizer seems to require contact
for its spread. Brachet (1923) found that it could not exert its
influence beyond a cut.

As development continues, the organized tissue becomes in
turn an organizer, influencing the development of adjacent tissue.
The anterior part of the neural plate folds over to form a brain,
and evaginations from the sides of the inturned plate extend
toward the now overlying ectoderm. In several species of

28 THE BIOLOGY OF THE AMPHIBIA

Amphibia, each evagination which becomes the optic cup of that
side induces a lens to form in the overlying ectoderm; foreign
ectoderm transplanted over the cup is similarly modified. Dur-
ing gastrulation in the urodele, but apparently earlier in some
species of frog (Brachet, 1927), but not in others (Schotte, 1930),
the potencies for many structures are localized in the ectoderm.
Areas which are to give rise to gills, balancer, nose, ear, hypophy-
sis, etc., are segregated according to a pattern which seems con-
trolled in the first place by the direction of growth of the dorsal
lip tissue. These ectodermal potencies greatly affect adjacent
tissues. Thus Harrison (1925) has shown that if ectoderm from
the region of the mandibular arch of Amby stoma maculatum

embryos is transplanted to
other parts of the body just
before the appearance of the
balancer, it will give rise to
this structure in these regions
(Fig. 14). The ectoderm takes
the lead in balancer formation
and seems to condense the
underlying intercellular ground
substance into a fibrillar mem-
brane which gives support to
the ectoderm. Harrison sug-
gests that this modifying in-
fluence may be a type of
enzyme action. As develop-
ment continues the balancer
attracts a twig from the mandibular branch of the fifth nerve. If
the balancer rudiment is transplanted to a posterior position it
may attract a twig from a more posterior nerve or even from
similar nerves in a frog tadpole.

Epigenesis. — Many other striking cases of the effect of one
tissue on the growth of another tissue have been demonstrated by
experimental embryologists. The parts of a structure may
effect one another during growth, while together they may mold
adjacent tissues or be influenced by nutritional or hormonal
conditions of the body. For example, the two common sala-
manders Amby stoma maculatum and A. tigrinum grow at different
rates and the latter reaches a much larger size than the former.
If the eye of A. tigrinum is transplanted during an embryonic

Fig. 14. — The influence of the ecto-
derm in balancer formation in Ambys-
toma. A supernumerary balancer
developed from ectoderm transplanted
from another individual shortly before
the normal appearance of its balancer.
B, balancer of host; B\, balancer devel-
oped from grafted ectoderm; LL.,
lateral line sense organs appearing in the
grafted ectoderm. {After Harrison.)

DEVELOPMENT AND HEREDITY

stage to the embryo of A. maculatum, it will continue to grow
in this new environment at its own specific rate and will reach
the same large size as the eye which was not transplanted
(Harrison, 1929). Three or four months after the operation, the
transplanted A. tigrinum eye is approximately double the size
of the A. maculatum eye of the host and demonstrates in a con-
vincing manner that even such matters as size may be deter-
mined by factors within the tissues of an organ. If the grafted
eye should be taken from an older animal, its growth is at first
retarded (Twitty, 1930). This is apparently due to the fact that
the body of the host had not yet developed to the point where it
could release the growth mechanism of the grafted eye. Even
though the potential size of the eye is determined by intrinsic
factors of the eye tissue, the realization of this potentiality
depends upon certain changing conditions of development in the
body of the host (Twitty, 1930).

If the lens ectoderm alone is transplanted from Amby stoma
tigrinum to A . maculatum embryos, a lens is produced which is at
first too large for the eye (Harrison, 1929). The growth of this
lens is retarded but it in turn stimulates the bulb to more rapid
growth so that it becomes 30 per cent larger in diameter than the
bulb of the control. The bulb may also have an effect upon the
lens, for if the lens ectoderm of A. maculatum is transplanted to
A. tigrinum, the lens which was at first too small for the bulb
retards the growth of the latter while its own growth is accel-
erated. The size of the trabecula which forms the lateral wall of
the brain case in the orbital region is influenced by the size of the
adjacent eye. If the eye of A. tigrinum is transplanted into the
site of an A. maculatum eye, the trabecula on this side shows a
marked enlargement throughout most of its length (Twitty,
1929).

The skeleton is of importance in phylogenetic studies, chiefly
because it is usually the only part of extinct species which is
preserved in the fossil and therefore serves as the only basis of
comparison with living forms. The close correlation between
the skeleton and adjacent tissues is not a chance relation. The
eye, as shown in the above experiments, controls the size of the
trabecula. The auditory vesicle migrating from the overlying
ectoderm induces the development of a cartilaginous capsule
about itself even when transplanted to the region of the eye
(Luther, 1925). The cartilaginous nasal capsules of Ambystoma

THE BIOLOGY OF THE AMPHIBIA

were shown by Burr (1916) to be dependent on the nasal sacs
for their conformation. In brief, the skull is not merely molded
by the paired sense organs; parts of it are unable to develop a
normal form unless the sense organs are present.

Cartilage usually arises in the mesenchyme by a condensation
and transformation of this mesodermic tissue. But the tissue
which produces the branchial arches of both urodeles and frogs
migrates for the most part from a portion of the neural crest.
The removal of this portion of the ectoderm or mesectoderm in
the branchial region results in marked deficiencies in the hyo-
branchial apparatus in urodeles (Stone, 1926). A similar opera-
tion in frog embryos has demonstrated that the mesectoderm
gives rise to Meckel's cartilage, the palatoquadrate, the supra-
and infrarostral cartilages, the anterior portions of the trabeculae,
and the hyobranchial skeleton exclusive of the basihyal and
second basibranchial (Stone, 1929).

P. T.

Fig. 15. — Part of the mechanism of metamorphosis in Rana pipiens. His-
tolysis of the operculum by the degenerating gills. The forelimb was removed at
an earlier stage. P., perforation; T., histolysized area. {After Helff.)

Secondary organizers are not confined to the ectoderm but are
located in various parts of the body. The potencies for limb
formation with the resulting cartilage and bone development are
first localized in the mesoderm and these influence the overlying
epidermis. The potencies for gill formation occur in the ento-
derm but they can act only on a limited portion of the ecto- and
mesoderm (Severinghaus, 1930). This influence of one tissue
upon another is not restricted to the earlier stages of develop-
ment. The frog tadpole during metamorphosis does not thrust
its forefeet through the overlying membranes by sheer force.

DEVELOPMENT AND HEREDITY

Helff (1926) has shown that the atrophying gills produce a sub-
stance which digests two neat holes in the confining cover (Fig. 15).
Further, the metamorphosing tadpole owes the formation of its
eardrums to the influence of the annular cartilages which come to
underly the integument of the ear region. Foreign integument

Fig. 16. — The effect of the annular tympanic cartilage on the formation of
the tympanic membrane. Skin transplanted from the back to the tympanic
region develops a tympanic membrane by the influence of the underlying tym-
panic cartilage. Skin from the tympanic region transplanted to the back fails to
develop a tympanum. B.G., back-skin graft; T.G., skin graft from tympanic
membrane region transplanted to the back; T.M., tympanic membrane. (After
Helff, O. M., Studies on Amphibian Metamorphosis, Physiol. Zool., Vol. I, No. 4,
adapted from Plate IV, Fig. 13.)

transplanted over an annulus is molded (Fig. 16) into a tympanum
(Helff, 1928).

Basis of Homology. — The induction of structures by organizers
of various grades is probably due to chemical substances, and
these may have different positions in such related types as the
frog and the newt. In Rana the roof of the archenteron persists
as the dorsal lining of the alimentary tract, a median strip of
topmost cells becomes the notochord, and the dorsal mesoderm
splits off from the roof on either side of this. In the newt, the
whole roof of the archenteron in the midline becomes converted
into notochord, and the gut is completed dorsally by the ingrowth
of yolk cells from the side. Undoubtedly homologous structures
such as the gut of the frog and the newt may thus differ consider-
ably in their manner of origin. The organ-inducing materials are
most probably homologous but their center of activity has been
shifted. Similar changes of position of organ-forming substances
in the developing embryo may have been responsible for
the different final positions of various parts such as the limbs
in frogs and urodeles. The somites which form these struct-
ures in the two types may be those nearer or farther from the
head, but the hind limbs of the first are nevertheless homologous
with those of the second in spite of these different muscle-segment
origins.

T.G.

B..G.

THE BIOLOGY OF THE AMPHIBIA

At an early stage of development the potencies for organ for-
mation may extend beyond the region which eventually gives
rise to a structure. This manifests itself in the tendency for
transplanted tissue to form more than it would in the course of
normal ontogeny. Thus, Adelmann (1929) found that a small
median piece of neural plate, removed from a newt or Ambystoma
embryo and transplanted into the body wall of another one, gave
rise to a single eye in addition to dorsal parts of the brain, while
the donor, nevertheless, possessed eyes and brain of normal
proportion. Hence, the anterior end of the neural plate of these
salamander embryos possesses generalized eye-forming potencies,
any portion of which is capable of forming an eye. A median
piece of the neural plate removed from its normal environment
and thereby released from the influences of surrounding parts
differentiates into an eye, although in the normal course of ontog-
eny this tissue would have had a different fate.

The organ-forming substances may produce their effects at
different times in different Amphibia. In the eggs of some frogs
the potencies are apparently localized earlier than in the newts
(Brachet, 1927), and this may be one of the reasons why the
mesoblastic pouches, obviously primitive structures, still appear
in the development of some urodeles but not in pouch form in the
frogs. On the other hand, two such closely related frogs as
Rana fusca and R. esculenta may differ considerably in the local-
ization of potencies. The first requires the presence of the optic
cup to induce lens formation, while in the second species the lens
is self-differentiating. There is some evidence that even in the
newt a certain amount of self-differentiation occurs in the neural
plate independent of the inturned dorsal lip (Lehmann, 1926), and
a sharp line cannot always be drawn between dependent and self-
differentiating development. In fact, some tissues may be under
some circumstances dependent and under others independent.
This principle of double assurance (Spemann, 1928) is probably
widespread in early stages of development.

Development of Limbs. — Further, there must be considered
the phenomenon that one axis of a structure may become fixed
before another. Thus, in the early limb buds of Ambystoma, the
dorsoventral axis can be inverted and yet the palm, as it develops,
will appear face downward, for the dorsoventral axis is not
established at this stage. The anteroposterior axis, however, is

DEVELOPMENT AND HEREDITY

fixed at the same stage and an inversion of the bud brings the
first digit, when it appears, in the position of the last (Harrison,
1921). This polarization of the anteroposterior axis resides in
the limb mesoderm and not in the surrounding tissue. Detwiler
(1929) showed that when the mesoderm of a forelimb of Amby-
stoma was inverted and grafted into slightly older embryos, a
limb with reversed asymmetry differentiated.

The determination of the anteroposterior axis of the limbs is
made long before they appear as rudiments (Detwiler, 1929).
The anterior extremities develop much later in Amby stoma tigri-
num than in A. maculatum; nevertheless the dorso ventral axis
of these limbs is determined at about the same time in the two
species (Ruud, 1926). Brandt (1927) finds that the fixation of the
limb axes of Pleurodeles, a primitive salamandrid, occurs at
approximately the same time as in Ambystoma. This is of
interest, for in Triturus, a more specialized salamandrid, this
fixation of limb axes occurs at an earlier stage of development.
The same is true of the shoulder girdle, its axes being determined
earlier in Triturus than in Ambystoma (Brandt, 1927). The
shoulder girdle and limb, in spite of their close functional correla-
tion, are determined independently, the latter at an earlier
stage of development than the former (Swett, 1928). It would
seem from these few cases that determination occurred earlier
in the more specialized species and that it was not correlated with
the time of appearance of the limbs, or with the period of girdle
determination.

The limb as it develops is subject to influences which may
modify it considerably. Schmalhausen (1925) showed that
malnutrition or abnormally high temperatures retarded the
development of the postaxial portions of the limbs of the axolotl.
In some cases a fusion of the tarsal or carpal bones may occur as a
result, either the tibiale with the mediale I, or the intermedium
with centrale, or certain tarsalia with one another or with the
fibulare. This was apparently due to the fact that growth and
morphogenesis were retarded more than histogenesis in these
regions. These observations invite a comparison with limb
development in salamanders which normally differentiate rapidly
and at a small size. In many of these, such as Manculus and
Hemidactylium, it is the postaxial part of the feet which has
suffered the greatest reduction.

THE BIOLOGY OF THE AMPHIBIA

Influence of Function. — Many structures, after they have
appeared as rudiments, are dependent on function for their
complete elaboration. If the legs of a tadpole are early removed,
the hind brain will remain stunted (Durken, 1912) ; if the eyes are
removed, the optic lobes of the brain become reduced (Steinitz,
1906). Constitutional growth factors of heart, gills, and
apparently of pronephros are readily modified if such organs are
transplanted to parts of the body where they may grow but
are unable, because of conditions there, to realize their normal
functions.

The influence of function is especially well marked in the
development of the nervous system. Excitations received from
the sense organs have an important influence on the growth of
the nerve centers in the central nervous system during each
ontogeny. In the cord, moreover, there is a proliferation and
arrangement of cells in response to the growth of descending
fiber tracts. Such a growth makes possible the individuation
of reflexes out of the primary behavior pattern. When function
is lost in the forelimb of Ambystoma, the cellular areas within
the branchial segments may be reduced to 60 per cent of the
normal (Nicholas, 1929), and this reduction is apparently due
to the failure of cell proliferation in the absence of descending
fiber connections.

The need of the functional stimulus of light for the retention
of a well-developed retina is discussed below in the case of the
Cave Salamander, Typhlotriton. There is no sharp separation
of the period when function will exert its effect from that when
chemodifferentiation prevails. Thus, the extent of muscular
development in the tail of tadpoles is apparently correlated with
the amount of exercise they receive, but the color change of the
tail skin which occurs at metamorphosis is inherent in the skin
and not produced by the degenerating tissue below. Tail skin
transplanted to the back undergoes the usual color change at
metamorphosis (Lindeman, 1929). The nervous system is not
indispensable for the development of limbs nor for the histo-
logical differentiation of its tissues (Mangold, 1929). A nerve-
less limb does not reach the size of a normal one and here lack of
function would seem to be exerting an influence.

During development there arises a series of organs which release
secretions having an effect not merely on adjacent tissues as in
the case of organizers but frequently on many parts of the body.

DEVELOPMENT AND HEREDITY

These are the glands of internal secretion such as the pituitary
and the thyroid. We shall consider them in greater detail in
another chapter, although some have an important influence on
development.

From this outline of the mechanics of development it is clear
that any one of many alterations of development might account
for the differences between two species. The integument of the
head of a frog might be able to produce a tympanum but if — due
to some modification of development — the tympanic annulus
were held at a distance from the integument, no tympanum
would develop. Brachet (1927) concluded from his experiments
with Rana fusca that the amount of gray crescent material
present in the egg at the time of fertilization determined the size
attained by the adult frog. It may be inferred from the work
of Uhlenhuth (1920) on salamanders that the amount of hormone
released by the anterior lobe of the pituitary of the growing
individual has an important effect on size. Burns and Burns
(1929), however, united embryos of Amby stoma tigrinum with
A . maculatum in pairs and noted that the larvae as they developed
retained their specific growth rates and grew to the size character-
istic of their own species. Thus, capacity for growth would
seem to be inherent in the tissues of a species, although the
addition or removal of some endocrine substances from the body
may influence the result (see Chap. XVIII). No doubt the
reduction or loss of some chemodifferentiators in the early
embryo is the immediate cause for the failure of certain structures
to appear. Thus, Harrison showed that ectoderm from the
balancer region of the early embryo Amby stoma tigrinum, which
usually lacks a balancer, if transplanted on the head of A.
maculatum, fails to induce a balancer in this species which
normally possesses one. There is something missing in the
ectoderm of the mandibular arch ectoderm of A. tigrinum
which is present in that of A. maculatum.

Although lack of function or of certain chemodifferentiators
at critical stages of development may be the immediate cause of
differences existing between two species, these embryonic condi-
tions are in turn determined by the specificity of the germ plasm
itself, which is provided by the chromosomes with their equip-
ment of genes. Every cell of the embryo's body has the same
complement of chromosomes as the fertilized egg. Develop-
mental changes are due to a progressive change in the cytoplasm,

36 THE BIOLOGY OF THE AMPHIBIA

and this change is produced presumably by the chromosomes in
the first place, since these alone are known to be the bearers
of hereditary characters. The establishment of the center of
rapid cell division in the gray crescent and the development of
gradients of cell activity from this center give the necessary
conditions for localizing potencies in different parts of the embryo
along these gradients. Once "the embryo in the rough" is
established, however, development is not merely an unfolding
of these potencies, for the tissues containing the potencies react
on one another and are modified by function and by environ-
mental influences. Every animal possesses more potentialities
than are ever realized; the conditions of development, and
especially the environment, determine what characters will
appear.

Regeneration. — Larval salamanders frequently snap off each
others' legs or gills if they are crowded together in dishes. Some
terrestrial salamanders, especially plethodontids, will leave part
of their tail in the hand which attempts to seize them. The
autotomy of the tail resembles that of many lizards, although it
is not so spontaneous as in the geckonids, and the split occurs
between the vertebrae instead of along an intra vertebral split.
Nevertheless, the tail of some plethodontids seems modified in
anticipation of its being lost, for a constriction occurs around its
base at the point where the tail readily breaks off. The lost
parts of both young and old are regenerated. The phenomenon
of regeneration seems to be a highly adaptive mechanism in
these aquatic larvae and terrestrial plethodontids, permitting
these forms to succeed under difficult conditions of livelihood.
Ability to regenerate is, however, not closely correlated with
liability to injury in Amphibia. Newts may regenerate their
hyoids (Bogoljubsky, 1924) and frogs their lungs (Westphal,
1925). The protected gills of tadpoles may regenerate, while
the exposed gills of axolotls may not attain on regeneration the
form of the original structures (Wurmbach, 1926). Natural
selection has played only a minor part in the distribution of the
capacity to regenerate. The latter is a common faculty of the
tissues of animals but one which has been reduced during phy-
logeny (Korschelt, 1927).

The power of regeneration diminishes with increasing organ-
ization usually during both ontogeny and phylogeny. Adult
newts can regenerate new limbs but do this more slowly than

DEVELOPMENT AND HEREDITY

larvae of the same species. In reptiles and especially in higher
vertebrates the capacity to regenerate is greatly restricted. The
Salientia on the other hand, which are more primitive than
salamanders in many features of their skeleton, show only slight
regenerative ability during adult life. Alytes can restore extremi-
ties if they are cut off just before metamorphosis, but even this
capacity is lost in the more advanced Salientia. Metamorphosed
frogs, however, have been reported to regenerate single digits
and partial limbs.

Relation of Regeneration to Development. — The tissues which
take part in regeneration may be derived from already dif-
ferentiated cells, but more usually undifferentiated cells are
marshaled together to form the new structures. The regenera-
tion of the lens illustrates well the first kind of regeneration.
Although the lens is formed originally from ectoderm under the
influence of the optic cup, it may regenerate from the iris in
both frogs and salamanders. The iris cells undergo a loss of
pigmentation, dedifferentiate, and develop a new type of structure
to form a lens. In the more usual type of regeneration, connec-
tive tissues form a mass below the surface of the wound and
begin to grow and differentiate in the manner of embryonic
tissues. Regeneration may be described as the induced develop-
ment of undifferentiated tissues.

The close relation of regeneration to development is well
shown in the recent work which has been done on the growth of
limbs in Amphibia (see reviews by Mangold, 1929; Korschelt,
1927; and Przibram, 1927). When the limb of a salamander
larva is cut off, the new limb bones develop not from the bone
rudiments in the stump but from the blastema growing over the
stump (Weiss, 1922). A boneless forelimb transplanted to the
back of a salamander will regenerate its proper bones (Bischler,
1926). A complete foot can develop from a cross-section of
only half an extremity. There is no part-for-part influence
even when regenerating bones and bone stumps lie adjacent to
one another (Weiss, 1925). The blastema lying above the
wound contains the determinants of the complete part within
itself. Weiss (1926) removed the skin from a limb stump and
covered it with lung tissue to prevent necrosis. The stump
regenerated skin as well as skeleton and musculature. Sections
revealed that the skin of the regenerated limb had no corium
in the part covered by the lung. Hence the corium of the

THE BIOLOGY OF THE AMPHIBIA

regenerated limb skin had apparently been derived, like the
skeleton, from the blastema of the stump.

Extremities have been induced to develop on the side of the
body at a distance from the original limbs by introducing
into the side portions of the otic capsules or pieces of celloidin
(Balinsky, 1926, 1927; Filatow, 1927). In these cases it would
seem that material from the normal extremity, either anterior
or posterior to the wound, had been attracted to the new wound
surface. These undifferentiated cells of the extremities in the
new locality become organizers of the surrounding material to
form a limb. G. Hertwig (1927) transplanted the limb buds of
haploid newt larvae on diploid individuals of the same species.
The haploid material partially degenerated through lack of
vitality and was replaced by diploid host cells. The diploid
tissue was thus organized by haploid limb rudiments. The
organizing center would seem to lie in the mesoderm and not in
the ectoderm as would appear to be the case of the balancer,
since covering of a limb rudiment by foreign ectoderm does
not prevent the development of mesoderm into extremities
(Detwiler, 1922; Ekman, 1922).

With the development of the limb rudiment, functional adjust-
ments between the parts take place. Although an extremity can
develop without a girdle (Brandt, 1926), or two girdles may be
present with one limb, secondary adjustments take place which
may be correlated with function during development. Brandt
(1927) showed that one girdle possessing two extremities will
develop two glenoid cavities or one wide one for the two heads
of the humeri. Swett (1926) found that the glenoid fossa did
not develop at all when the extremity was absent. Although
the nerves are not necessary for the early growth of the limbs,
they appear necessary for the full elaboration of these structures.
If the nerves are prevented from growing into the limb bud, the
latter differentiates normally, but the resulting limb is 10 per
cent shorter and 50 per cent narrower than normal limbs. The
atrophy is most marked during the functional stage. Hence,
function has an important influence on the quantity of tissue
and on the maintenance of its form.

When a limb regenerates from the base of another one and
forms a duplication, the secondary limb is usually a mirror image
of the primary limb. This has been explained by assuming that
every extremity anlage has the potentiality of forming two mirror

DEVELOPMENT AND HEREDITY

image extremities, but normally one of these is inhibited by the
growth of the other. Triplicate formation of limbs may be
experimentally produced, however, making further assumptions
necessary. A simpler explanation assumes that the anterior-
posterior axis of the secondary limb rudiment is influenced
by the primary limb and develops as a mirror image of it. The
dorsoventral axis is determined by the factors at the base of the
growing limb. Since the anteroposterior axis of the limbs,
whether primary or secondary, is generally determined in
Amphibia much earlier than the dorsoventral, a reversal of the
lateral quality is induced by the inversion of the antero-
posterior axes of the secondary buds (Swett, 1927). The deter-
mination of the axes in regenerating limbs would, according to
this explanation, follow the same course as in normal develop-
ment, with an interval between the determination of each of the
axes. The effect of injuries which produce duplications consists
in the weakening of the dominance in the limb center so that one
or, rarely, more peripheral regions of the rudiment become
independent and sprout as additional limbs.

Regenerative Capacity. — The regenerative capacity is greater
in the tail than in the extremities and greater in the posterior
than in the anterior limbs (Ubisch, 1923). This may be due
to the fact that the posterior regions are growing more actively
than the anterior. The foot of the toad loses its power of
regeneration at a stage before it is completely differentiated,
while the newt, as stated above, conserves the power of regenera-
tion its entire life. It has been suggested that the salamander
limb may contain more undifferentiated cells than the developing
limb of the toad, but there is little histological evidence in
favor of such an assumption. The factors which have brought
about the restriction of the regenerative capacity in some
groups of Amphibia but not in others are still unknown. Many
factors influence the rate of regeneration. If the wound surface
is sewed together or its healing hastened, regeneration may
be prevented or delayed in salamanders (Schaxel, 1921). Swim-
ming movements not only hasten the regeneration of the
tail but may actually prevent its growth in an oblique direction
(Harms, 1910). If function has such a marked effect on the
regeneration of the tail, it probably has an equal effect on its
normal growth. Hormones which influence growth affect
regeneration. Thyroidectomy retards the regeneration of the

40 THE BIOLOGY OF THE AMPHIBIA

hind limbs of salamanders (Walter, 1911), while hypophysectomy
prevents the regeneration of limbs and tail in the adults (Schotte,
1926). Since large losses up to a certain limit are repaired more
rapidly than small ones, there is apparently an increase in
the energy of regeneration with increase in the size of the
wound.

The regenerative repair of injuries may lead to many kinds
of growths in Amphibia. Salamanders may develop forked
tails, extra digits, or complete supernumerary limbs. The
healing of wounds represents a type of regeneration. After
blood clotting, the epithelial cells of the edges of the wound
grow out over the exposed surface. If a young Necturus is
beheaded, the wound heals and the body may continue to grow
and differentiate for two months (Eycleshymer, 1914). Struc-
tures which regenerate show no decrease in the rate of regenera-
tion after successive removals (Zeleny, 1916).

Regeneration is a type of developmental regulation which
results in the replacement of parts normally lying peripherally
to the cut surface. In adult Amphibia the body is a mosaic of
regenerative territories, having different morphological potential-
ities. The complete extirpation of one of these regions prevents
its regeneration. Transplanting it to some other part of the body
does not destroy its specificity (Guyenot and Ponse, 1930).

There are other types of regulation which may be confused
with regeneration. If a limb bud is split in the growing larva it
will develop into two limbs. The latter phenomenon is com-
parable to the twinning produced by restricting the fertilized
egg of the newt in the midline during the two cell stage.

Hybridization. — Hybrids between different species, genera,
and even families of Amphibia, have been reported, but such
individuals rarely grow to maturity and in many cases may be
false hybrids resulting from the activation of the egg by the sperm
without the transmission of the paternal characters. The
European newts have been the most extensively hybridized.
A large percentage of the species have been successfully crossed
by Wolterstorff, Schreitmuller, Poll, and others (Schreitmuller,
1912). In some cases species which have never been known to
cross in nature produced true hybrids in the laboratory tanks
(Schreitmuller, 1913). Newts carry the spermatozoa for long
periods in the spermatheca of the female and possibly also in
the oviduct where fertilization occurs. Hence, the identifica-

DEVELOPMENT AND HEREDITY

tion of the young as the offspring of any particular male becomes
often difficult. In some cases hybrids may be recognized by
the appearance of specific characters of the male in the offspring.
True hybrids with characters of the male species have been
produced various times among European newts, perhaps most
recently by Bataillon (1927). There seems to be no doubt that
very distinct species of Triturus are able to hybridize.

European Salientia have frequently been crossed. As long
ago as 1883, Heron Royer described hybrids of the interfamily
cross Rana fusca X Pelobates fuscus as exhibiting characters of
both parents. Crosses between different species of Discoglossus
and between species of Bufo gave hybrids with some male char-
acters (Heron-Royer, 1891). The hybridization of various
European Salientia and newts had recently been carefully
studied by Hertwig (1918), who finds that true hybrids result
from crossing a number of different species. Among the frogs
studied, only Rana arvalis 9 X R. fusca ^ and Bufo communis
9 X B. viridis *b developed into healthy adult hybrids. Crosses
between Bufo and Rana gave, in some cases, true hybrids which,
however, developed poorly. Usually the intergeneric and most
interfamily crosses, if successful, developed into false hybrids,
the male nucleus not entering into the cross. This was shown in
hybrids of Bufo communis 9 X Pelobates fusca 'b where the nuclei
of the body cells were only half the size of those of normal toads
and hence were presumably haploid. In other cases, however,
they were of the normal size and presumably diploid. Similar
full-sized nuclei may appear in the progeny produced by irradiated
sperm. As previous experiments had shown such sperm not to
be functional, the diploid number of chromosomes had apparently
been restored by a doubling of the maternal set of chromosomes.
A similar restoration of the diploid number may occur in eggs
developing parthenogenetically after pricking with a needle
(Parmenter, 1920). From the work of Hertwig (1918) it would
seem that most cases of intergeneric crosses were cases of activa-
tion by the spermatozoa without union of the hereditary material.
Apparently, the nuclear material of widely separated species is
incompatible and unable to enter into the formation of a zygote.
This makes it especially important that the few reported cases
of true intergeneric crosses should be confirmed. In no such case
was an anatomical study made to determine how the generic
characters combined.

THE BIOLOGY OF THE AMPHIBIA

Hybrid Salientia frequently develop slowly and often die at
gastrulation when growth takes place at the expense of the
yolk. Apparently the sperm nucleus in the foreign egg is unable
to utilize the foreign yolk. Cell size varies with the species and
the difference may be considerable in such closely related species
as Bufo vulgaris and B, viridis. Hertwig (1930) suggests that
the quantity of nuclear material available is a factor regulating
the rate of yolk elaboration. If the nuclei transmit specific
developmental potencies quantitatively proportional to their
volume, one of the chief reasons for the failure of hybrids
to develop may lie in this quantitative difference be-
tween available nuclear material and amount of yolk to be
elaborated.

The study of hybridization has an important bearing on the
origin of species. The hybrid between the European newts
Triturus cristatus and T. marmoratus was described as a distinct
species, T. blasii. Rollinat showed that hybrids were fertile
inter se and with the parent stock (Boulenger, 1898). T. blasii
occurs in France where the ranges of the two parent forms overlap.
It is not considered a distinct species by some systematists.
As discussed in another chapter, the criteria of a species are
frequently difficult to define.

Frogs and toads combining the characters of two very distinct
species are sometimes found in regions where the ranges of these
forms overlap. These have sometimes been considered hybrids.
Examples may be found among the African tree frogs which have
been called Leptopelis tessmanni (Noble, 1924) and among the
African toads described by Power (1926). In none of these cases
have breeding experiments confirmed the hybrid character of
these individuals.

Although experimental evidence is lacking, it seems certain
that hybridization often occurs in nature where the ranges of
two closely related subspecies overlap. Museums contain many
specimens which cannot be more definitely assigned to one
species than to the other. Crossing makes possible the recom-
bination of characters and if the environment permits such
hybrids to isolate themselves until a stock is well started, a new
form may arise. This subject will be discussed more fully
below. Aside from theory, the material available in museums
suggests that hybridization of subspecies is a far more frequent
phenomenon in nature than the crossing of species.

DEVELOPMENT AND HEREDITY

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Bedeutung des ektodermalen Epithels der Extremitatenknospe von
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Steinitz, E., 1906: tlber den Einfluss der Elimination der embryonalen
Augenblasen auf die Entwicklung des Gesamtorganismus beim Frosche,
Arch. Entw. Mech., XX, 537-578.

Stohler, R., 1928: Cytologische Untersuchungen an den Keimdrusen mittel-
europaischer Kroten (Bufo viridis Laur., B. calamita Laur., B. vulgaris
Laur.), Zeitschr. Zellforsch. mikr. Anat., VII, 400-475, pis. IX-XIV.

Stone, L. S., 1926: Further experiments on the extirpation and transplanta-
tion of mesectoderm in Amblystoma punctatum, Jour. Exp. Zool.,
XLIV, 95-131.

, 1929: Experiments showing the role of migrating neural crest

(mesectoderm) in the formation of head skeleton and loose connective
tissue in Rana palustris, Arch. Entw. Mech., CXVIII, 40-77.

Swett, F. H., 1926: On the production of double limbs in amphibians, Jour.
Exp. Zool, XLIV, 419-473.

, 1927: Differentiation of the amphibian limb, Jour. Exp. Zool.,

XLVII, 385-432.

, 1928: Studies on the shoulder-girdle of Ambystoma punctatum

(Linn); I, Determination of its do rso ventral axis, Jour. Exp. Zool.,
LI, 389-402.

Twitty, Victor C., 1929: Correlation in development of structures associ-
ated with transplanted eyes, Proc. Soc. Exp. Biol. Med., XXVI, 726-727.

■ , 1930: Regulation in the growth of transplanted eyes, Jour. Exp.

Zool, LV, 43-52.

Ubisch, L., 1923: Das Differenzierungsgefalle des Amphibienkorpers und
seine Auswirkungen, Arch. Entw. Mech., LII, 641-670.

Uhlenhuth, E., 1920: Experimental gigantism produced by feeding pitui-
tary gland, Proc. Soc. Exp. Biol. Med., XVIII, 11-14.

Vogt, W., 1926: Die Beziehungen zwischen Furchung, Hauptachsen des
Embryo und Ausgangstruktur im Amphibienei, nach Versuchen mit
ortlicher Vitalfarbung, Sitz. Ges. Morph. Physiol. Munchen, XXXVII,
60-70.

DEVELOPMENT AND HEREDITY

Walter, F. K., 1911: Schilddriise und Regeneration, Arch. Entw. Mech.,
XXXI, 91-130.

Weber, A.. 1922: La fecondation chez la salamandre alpestre (Sal. atra

Laur), Compt. rend. Ass. Anat., XVII, 327-329.
Weiss, P., 1922: Unabhangigkeit der Extremitatenregeneration vom

Skelett (bei Triton cristatus), Anz. Akad. Wiss. Wien, LIX, 231-3.
■ , 1925: Unabhangigkeit der Extremitatenregeneration vom Skelett

(bei Triton cristatus), Arch. mikr. Anat. Entw. Mech., CIV, 359-394.
, 1926: Morphodynamik; Ein Einblick in die Gesetze der organischen

Gestaltung an Hand von experimentellen Ergebnissen, Abh. Theor. Biol.

Schax., XXIII.

Westphal, Kurt, 1925: tlber Lungenregeneration bei Anurenlarven,

Zeitschr. Anat. Entw., LXXVII, 144-163.
Wintrebert, P., 1929: La digestion de l'enveloppe tubaire interne de l'oeuf

par des ferments issus des spermatozoldes et de l'ovule chez Discoglos-

sus pictus Ottb, Compt. rend. Acad. Sci., CLXXXVIII, 97-100.
Wurmbach, H., 1926: tiber Kiemenregeneration beim Axolotl, Zool. Anz.,

LXVII, 309-322.

Zeleny, Charles, 1916: The effect of successive removal upon the rate of
regeneration, Proc. Nat. Acad. Sci. Wash., II, 487-490.

CHAPTER III
THE MODE OF LIFE HISTORY

Many Amphibia do not lay their eggs in water as in the case
of Rana and Ambystoma but deposit them on land and some-
times even in nests constructed by one or both parents. The
eggs and larvae which develop in these situations are often
modified in adaptation to their surroundings. It has recently
been recognized that these modifications have usually evolved
slowly and the various steps by which extreme stages have been
reached may often be still found in related species. The mode
of life history and the modifications of eggs and larvae thus
often give clear evidence as to the affinities of a species.

Cryptobranchidae. — The American giant salamander, Crypto-
branchus alleganiensis, lays its eggs in two long chains (Smith,
1912). Fertilization is external and the larvae which escape
from the egg capsules are short limbed with no dorsal fin on the
body and no balancers such as occur in Ambystoma. Have these
characters any phylogenetic significance? Cryptobranchus, as
far as known, has exactly the same life history as Megalo-
batrachus, the giant salamander of Japan and China. These
two genera belong to the same family and hence only one type
of life history is found throughout this family. The Crypto-
branchidae, moreover, have been derived from the Hynobiidae
and may be considered merely permanent or partly meta-
morphosed hynobiid larvae of large size. The hynobiids are
the only other salamanders (except the Sirenidae) which practice
external fertilization. All of the genera lay their eggs in two
sacs and, although these are not so elongate as the egg chains of
Cryptobranchus, and consequently have thicker walls, they
have much in common. Hynobius, the least specialized genus
of the family, lays some 35 to 70 eggs, 2.5 to 3.2 mm. in diameter,
within each egg sac. The younger larvae, as far as known, are
all Ambystoma-like, with dorsal fins, balancers, and long external
gills. The eggs are laid in ponds, temporary pools, springs, or
even slow-moving streams. Within the family there are two

THE MODE OF LIFE HISTORY

genera which live in or near mountain brooks. The egg sacs
of one of these, Ranodon, are fastened to the under sides of flat
stones, beneath which water flows. The eggs are larger than
those of Hynobius and fewer in number. The larvae hatch in
a more mature condition, and their digits are shorter than in
that genus. Apparently the dorsal fin is also reduced (Schmal-
hausen, 1917). In Onychodactylus there is no dorsal fin and
the digits are not only short but are equipped with horny claws.
Further, their external gills are comparatively short. It is
apparent that the Cryptobranchidae have received their method
of fertilization and general character of their egg capsules from
the family Hynobiidae as a whole, while their short gills, reduced

Fig. 17. — The principal types of urodele larvae. A. Terrestrial type: Pletho-
don vandykei. B. Mountain-brook type: Dicamptodon ensatus. C. Pond type:
Amby stoma paroticum.

fins, and short toes may have been inherited from mountain-
brook ancestors, presumably of the same family. Apparently
also the large eggs (although not particularly large when com-
pared with the body length of the parent) may also be considered
a mountain-brook inheritance. These large eggs and " swift-
water features" of the larvae frequently appear in species of other
families of salamanders (Fig. 17) which live in mountain brooks.

THE BIOLOGY OF THE AMPHIBIA

It is difficult to tell a priori which character will prove the most
conservative in evolution, but in general the more specialized a
structural modification may be the greater is the probability
that it will be modified only gradually during evolution.

In all the higher salamanders except the Sirenidae, fertilization
is internal. Very little is known about the breeding habits of
Siren and Pseudobranchus, except that the eggs of both are
large, pigmented, and laid singly or in small groups. The lar-
vae of both, soon after hatching, have elongate bodies approach-
ing the form of the adult. This in itself would suggest that the
Sirenidae is an isolated group. The larvae of both genera, as
they mature, have the ability of reducing their gills to mere
stumps if respiratory conditions in the aquatic medium are not
suitable to them. This is not a metamorphosis but merely a
temporary loss of the gills. The larvae never undergo a com-
plete metamorphosis although, as discussed under the heading
of this subject (page 103), they normally transform certain
structures, especially the integument in Siren.

Proteidae. — The Proteidae, which includes the well-known
genus Necturus, are also somewhat isolated structurally from
other salamanders and, like the Sirenidae, never complete their
metamorphosis. The two genera Necturus and Proteus of
this family agree in laying their eggs singly in the water, attached
to the under surface of rocks, boards, or other objects in still
water; but they have also been recorded in streams. Since the
habit of selecting the under surface of rocks is common to
mountain-brook salamanders of two other families, it is possible
that the Proteidae may have arisen in mountain brooks. In
fact, Proteus in its subterranean habitat must be subject to a
current for a considerable part of its life. Further, the eggs
of both genera are large and the larvae are devoid of dorsal fins
and have short limbs. These mountain-brook characters, if
such they be, are common to other larvae living in a similar
habitat and hence give no clue as to the ancestors of these genera.
In this case we do not have extreme larval modifications pointing
the way to relationships, but as both genera of the family have
the same mode of life history in spite of the fact that the adults
occupy totally different regions, we have further evidence of
the stability of breeding habits in phylogeny.

Proteus, under certain conditions, does not lay eggs but retains
them in its oviducts where one or two may undergo their develop-

THE MODE OF LIFE HISTORY

ment, finally to be born as salamanders resembling their parents
in most particulars. No especial modifications of either the
larvae or of the oviducts are known to occur to permit this change
in the mode of life history. The phenomenon is very similar to
the case of some species of lizards, such as certain horned toads
which may either lay eggs or give birth to their young alive.
The phenomenon is, however, very rare in the salamanders and
very much in need of further study.

Ambystomidae. — The best-known genus of American sala-
mander is Ambystoma. Most of the common eastern species,
maculatum, tigrinum, and jeffersonianum, lay their eggs in the
water in early spring, but opacum lays them in the fall on land,
and the female curls about them. The young, which hatch on
the advent of the rains, make their way into the water and
have all the larval characters of the other species of the genus.
These are the broad body and tail fins, the balancers (rarely
absent), and the elongate gills, each provided with a central
rachis and many pairs of filaments. The middle- western A.
annulatum lays its eggs in the water (occasionally on land), and
the larvae, as far as is known, resemble the other species of the
genus. The Ambystoma larvae are similar to those of Hynobius,
and the eggs of some species are laid enclosed in a common
gelatinous capsule, apparently resembling the egg sacs of Hyno-
bius but not so elongated. The Ambystomidae are closely
related to the Hynobiidae but they have advanced beyond that
group in developing a complex mechanism for internal fertiliza-
tion. Nevertheless, the mode of life history seems to have been
evolved out of a type common to the most primitive genus of
that family. The Ambystomidae include two mountain-brook
genera, Rhyacotriton and Dicamptodon. The latter of these
lays small clumps of eggs in the cool lakes of the west coast of the
United States (Storer, 1925). The egg capsules, which are two
and three in Ambystoma, are apparently reduced to one in this
species. The larvae, at least in some part of the species range,
make their way into mountain streams where they assume all
the characters of the mountain-brook larvae discussed above.
Rhyacotriton lays large pigmentless eggs attached singly to
stones. It is a much smaller salamander than Dicamptodon
and like many other dwarf forms lays fewer eggs than its larger
relative. The larvae which hatch from the eggs possess the
mountain-brook characters of Dicamptodon larvae. Rhyaco-

THE BIOLOGY OF THE AMPHIBIA

triton and Dicamptodon are more closely allied to one another
than they are to Ambystoma, and their larval characters tend to
confirm this relationship.

Ambystoma has one larval character which is found elsewhere
among salamanders only in the hynobiid Onychodactylus.
Anterior to the teeth on the lower jaw, there is found a horny
beak very similar to the larval mandible of frog tadpoles. This
beak has been described only in the axolotl and in one species of
Onychodactylus, but it is so distinctive a structure that probably
it will be found in other species of these families. The Sirenidae,
which may possibly have had hynobiid ancestors (Noble, 1929),
have developed horny sheets on both jaws. Since no other
salamanders have horny jaws, we may consider this character
as evidence that the forms are related.

Salamandridae. — The Salamandridae seem to have evolved
from some prehynobiid stock, for the most primitive genera
differ markedly from Hynobius in structure. These primitive
genera, Tylototriton, Pleurodeles and some species of Triturus,
lay their eggs in loose chains or short bunches very similar to
the eggs of Ambystoma tigrinum. The larvae which emerge
from them have the dorsal fins, broad tail, and long gill character-
istics of Ambystoma. The other newts were apparently derived
from this primitive stock which seems to have been widespread
in both Asia and Europe. The pond species lay their eggs
singly, attached to water weed. This habit of laying single
eggs appears as a variation in Triturus torosus and Ambystoma
tigrinum. Differences occur in the various species. The
American newt, T. viridescens, lays small eggs, approximately
1.5 mm. in greatest diameter and spherical in shape. Each is
enclosed in a more or less oval mass of jelly which during the
later period of development is well separated from the egg by a
fluid, oddly enough of a greenish color. The American newt is
also distinctive in that the female usually wraps a leaf about the
single eggs which further protects them. Although all the more
specialized pond newts lay single eggs, there are various specific
differences in the form of the egg capsule, shape of the egg, and
method of oviposition.

The mountain newts of Europe are sometimes referred to a dis-
tinct genus, Euproctus. The eggs are slightly larger than those
of most pond newts, averaging approximately 2.5 mm. in diameter
without the egg capsule in the case of E. asper. The eggs are

THE MODE OF LIFE HISTORY

laid singly on the under side of stones in running water. Despax
(1923) has suggested that the large egg size of the latter may be
due to the cold water in which the eggs are laid and he has drawn
a comparison in the egg size of certain cold- and warm-water
fish. The American newt, Triturus viridescens, will lay its eggs
on stones if no vegetation is available (Moesel, 1918), but they
are not laid under the stones and, of course, are not of larger size.
Mountain-brook salamanders of all families tend to reduce their
lungs and develop habits of crawling under stones in the water.
Hence, the method of egg laying found in Euproctus was prob-
ably evolved out of the method found in the pond newts, the
change of egg-laying site being conditioned by the changed habits
of the adult. The larvae as they develop have short external
gills and lack the dorsal fins, thus representing another instance
of convergent evolution in the mountain-brook habitat. In
the frogs and toads there are many instances where the method
of oviposition is more important than the larval characters.
The reason for this is that yolk size has changed frequently in
evolution and has necessitated marked change in the details
of development in closely related forms.

An instance of this fact may be seen in the European land
salamanders. Wunderer (1910) describes various differences
between the embryos of two species of Salamandra and is inclined
to believe that they are not closely related. Salamandra sala-
mandra and S. atra, however, both retain the eggs for a part of
their development within the female body. The larvae of both
species as they develop are equipped with long filamentous gills
which absorb oxygen from the highly vasculated oviducts
(Fig. 18). S. atra gives birth to fully metamorphosed young,
while S. salamandra usually gives birth to larvae, although some
individuals from Spain have been found to produce metamor-
phosed young as well. S. atra, being equipped with less yolk,
secures some nutriment from its parent's body during develop-
ment but it develops no especial mechanism for accomplishing
this act other than the elongation of the gills. Both species, as
they develop, exhibit one larval character which shows that both
forms have been derived from pond-breeding ancestors. A
rudimentary balancer appears in both forms while within their
parent's oviduct. Balancers have been recorded only from
pond-living salamander larvae, never from mountain-brook
forms. Further, Escher (1925) reports lateral-line organs, a

THE BIOLOGY OF THE AMPHIBIA

character of pond larvae, in S. atra. Hence, certain larval
characters in Salamandra indicate that these species are closely
related, the method of carrying their eggs until the young are
well advanced further supporting this conclusion. The dif-
ferences between the early embryos are brought about by dif-
ferences in amount of yolk. When the Amphibia are considered
as a whole, many other instances may be found where yolk size
has changed apparently suddenly in phylogeny. For example,
in the Marsupial Frogs, Gastrotheca, the species carry their eggs

Fig. 18. — A. Section through the wall of the oviduct of a gravid Salamandra
salamandra showing proximity of capillaries to lumen of the duct. B. Larva
removed from oviduct of a gravid female. Cap., capillary.

in sacs on the back of the female, and the larvae as they develop
have extraordinary bell-shaped gills. If the eggs are small-yolked,
the embryos soon assume the characters of tadpoles; while if
considerable yolk is present, they develop directly into froglets.
In either case both the character of the gills and the method of
carrying the eggs are evidence that the species are related.
Further, when the phylogeny of the group is considered, it is
found that the ancestral forms, which are grouped in the genus
Cryptobatrachus, all have large-yolked eggs. Hence, in this
case it would seem certain that the small-yolked eggs were derived
from the large-yolked ones. Similarly, there is considerable
evidence that the high mountain Salamandra atra, with its small
eggs, has evolved from the large-egged S. Salamandra of the low
altitudes.

THE MODE OF LIFE HISTORY

Amphiumidae. — In making comparisons of life histories there
is always the danger that the likenesses are due to superficial
resemblances. For example, the large American salamander,
Amphiuma, lays its eggs on land and the female curls about them.
This method is essentially like that of the Dusky Salamander,
Desmognathus fuscus, although the detailed character of the eggs
is different. The eggs of Amphiuma are laid in long rosaries,
while in a branched clump in Desmognathus. Amphiuma has
been derived from Salamandridae, while the Plethodontidae,
which include Desmognathus, arose from the same stock. The
mode of life history in many cases does not establish but merely
suggests where the relationships actually are to be found. The
anatomy of the adults must be considered in reaching a final
conclusion. The allantoic placenta is characteristic of the
placental mammals, but it occurs again in certain skinks but
not in all lizards. In any case the more specialized the modifica-
tion the better is the chance of its being the same in related
groups.

Plethodontidae. — The Plethodontidae, which embrace the
majority of North American salamanders, afford an excellent
illustration of the close correlation of change in life history with
change in phylogeny. The family evolved from the Salaman-
dridae, and some of the primitive genera of both lay their eggs
under stones in running streams. Each plethodontid egg is com-
paratively large, unpigmented, and attached separately by a
gelatinous stalk. The eggs are usually crowded together on the
under side of a single stone, and in some cases, at least, the female
parent remains near them. Apparently some of the primitive
plethodontids have departed somewhat from this method.
Gyrinophilus and Eurycea, as well as Pseudotriton ruber, retain
this primitive mode of egg laying inherited from mountain-brook
salamandrids. P. montanus, according to Brimley (1923), lays
its eggs singly or in small groups on dead leaves in the outlets of
springs. This species, unlike its relative P. ruber, is partial to
muddy springs, and hence a breeding site like th'at selected by
the stream forms might not be available to it in this habitat.
Further data are needed concerning the breeding of P. montanus
before the degree of divergence in the mode of life history may be
determined. Manculus, a dwarf derivative of Eurycea, lays
relatively large, pigmentless eggs, attached by short stalks to the
under sides of leaves in flowing spring water.

THE BIOLOGY OF THE AMPHIBIA

The commonest plethodontid salamander in eastern United
States is Desmognathus, the Dusky Salamander. This genus is
particularly interesting because within it there is found a gradual
evolution of the mode of egg laying from the ancestral condition,
where eggs are laid under stones in the water, to a terrestrial
condition. Although all adults live both in and out of water, the
progressive change in the mode of egg laying closely follows the
phylogeny of the group. The most primitive species is D.
quadra-maculatus, a large and powerful species of the southern
Appalachians. D. phoca, which is rather more advanced in
structure, lays its eggs in a similar manner but apparently always
deposits out of water. The common Dusky Salamander, D.
fuscus, which is still more specialized, lays its eggs in one or two
grapelike clusters in small excavations in the soft earth, beneath
stones or logs. The excavation is generally one or two feet from
the water. This is an advance over the primitive methods of the
larger species of the genus, not only in the form of the egg capsules
but also in the life history of the young. The recently hatched
individuals remain for 15 or 16 days on land, or at least with their
heads out of the water. These terrestrial young show various
adaptations to their habitat. The posterior limbs are longer in
proportion to the trunk region than during any other period in
later development. The tail lacks a fin. In brief, the young
Dusky Salamander, during the first two weeks of its life, is not
merely a little larva which chances to be hatched at a distance
from its aquatic habitat, but it is a terrestrial salamander fully
able to move about in the damp cracks and crannies leading from
the nest to the nearest pool. In the most terrestrial form of the
genus, namely D. fuscus carolinensis, the breeding site and appar-
ently the mode of life history remain the same. This illustrates
the general rule that salamanders do not lay their eggs wherever
they happen to be but that during the breeding season they move
into environments which are most suitable to the egg-laying
requirements. Further, the mode of life history gradually
changes in phylogeny and this change, while moving toward
terrestrialism, does not progress so fast as the change in habitat
preference exhibited by the adults.

In spite of this rapid change in breeding-site preference and
of adaptive changes in the young, certain larval characters appear
which stamp the group as related. The young of Desmognathus
fuscus, after its sojourn between land and water, finally takes up a

THE MODE OF LIFE HISTORY

purely aquatic life and develops the tail fin and gills of a mountain-
brook larva. It lives in the same streams as Eurycea bislineata
but may be distinguished from that species by its differently
formed gills. It has three pairs, as most of the salamanders
have, but these are devoid of a distinct central ramus so charac-
teristic of Eurycea and Gyrinophilus. There are only from three
to seven branches to each gill in the brush projecting from a cen-
tral axis. This shows that while swift currents may oppose a
limit to the growth of gills, probably for the good reason that cold
swift water is better supplied with oxygen than most pond water,
nevertheless, the character of the gills is determined by the
heredity of the species and, in the case of Desmognathus, affords
one of the best identification marks of the larvae. It does not
follow that gill structure in other groups will always afford impor-
tant clues as to relationships.

Terrestrial Plethodontids. — Another common salamander in
the eastern United States is Plethodon cinereus. It is a terrestrial
form and during the breeding season apparently shows a prefer-
ence for coniferous woods. The female lays from 3 to 12 large,
white eggs in a single mass, usually in crannies in the logs. The
egg cluster is usually attached to the roof of the cavity, each egg
being laid separately adhering to those previously laid, the
fused outer capsule seemingly forming a single envelope. The
embryos develop rapidly and soon show large external gills.
These are lost on hatching, when the young have the same form
as the adults. This same mode of life history is apparently
found throughout the entire genus. One of the most primitive
species is the large, slimy salamander, P. glutinosus, which has
been found to lay its eggs deep underground in the walls of caves.
In such situations there is an abundant water supply; neverthe-
less P. glutinosus has exactly the same mode of life history as its
smaller relative P. cinereus, even to the details of egg-capsule
structure and gill form. P. glutinosus, being a larger form,
lays more eggs; larger species of all genera usually lay more eggs
than smaller species of the same group. The immediate ancestors
of Plethodon seem to have been lost, but the mode of life history
practiced by the genus may be evolved from the pattern found in
the more terrestrial species of Desmognathus.

Plethodon has given rise to a number of derived groups. Some
of these genera, such as Aneides and Batrachoseps in the West,
are considerably specialized but nevertheless retain the mode

THE BIOLOGY OF THE AMPHIBIA

of life history found in Plethodon. Differences appear in the
form of the gills and, as discussed in Chap. VIII, may be correlated
with the increased efficiency of the blood of Batrachoseps
as a carrier of oxygen. It is perhaps not surprising that Batra-
choseps has very small external gills while Aneides has them not
only elongated but fused at the base to large leaflike structures.
Incidentally, Aneides aeneus, which in the character of its skull
is the most primitive member of the genus, has its gill form inter-
mediate between that of Plethodon and Aneides lugubris.
Other differences appear in the form of the egg capsules: while
the eggs of both Plethodon and Batrachoseps are attached to
one another and each egg surrounded by three capsules, those of
Aneides are separate and attached by a single twisted peduncle
to the roof of the nest chamber. In Ensatina, another derived
genus, the eggs are stuck together and only one egg capsule has
been recorded. Hence, while differences exist in both the char-
acter of the egg capsule and the gills of the young, all the species
agree in laying their eggs on land, there to develop directly into
salamanders without going through an aquatic period. This
mode of life history is not merely a consequence of the terrestrial
habit of the adults; other terrestrial salamanders, such as
Amby stoma opacum, have a very different life history.

Not all the derivatives of Plethodon have retained this
mode of life history. The four-toed salamander, Hemidactyl-
ium, seems structurally very closely allied to Plethodon but
is obviously a derived and not an ancestral form, because it
has only four toes on its rear feet and a double constriction
around the base of the tail. Both of these characters represent an
advance over the conditions in Plethodon. Hemidactylium
lays its eggs on land near sphagnaceous or at least wooded ponds.
The female twists her body around and attaches the eggs to
strands of moss lying over her head. This habit is found in
Plethodon but also in Eurycea which lays its eggs on the under
side of stones. The eggs are more numerous than with Plethodon
and the larvae which hatch out make their way into the adjacent
water. The eggs without their capsules are from 2.5 to 3 mm.
(Bishop, 1919), while those of Plethodon cinereus vary from 3.5
to 4.5 mm. in diameter. The yolk is very early absorbed by the
larva of Hemidactylium which develops a low dorsal fin approach-
ing that of many other pond salamanders in form (Fig. 19)
but not found elsewhere in the Plethodontidae. The larva does

THE MODE OF LIFE HISTORY

not, however, develop the balancer or elongate digits of primitive
pond salamanders and hence is merely a " plethodontid larva"
with a low dorsal fin. It has been suggested that the life history
of Hemidactylium may be explained by assuming that Plethodon
was originally aquatic or at least laid its eggs in the manner of
Eurycea and that the life history of Hemidactylium is a retention
of this primitive condition. It seems more likely, however, after
a consideration of the yolk reduction of Salamandra atra and some

Fig. 19. — The larva of Hemidactylium scutatum.

Marsupial Frogs, that the aquatic period in the life of Hemi-
dactylium is a derived condition induced by the reduction and
early absorption of the yolk in the embryos.

The European cave salamander Hydromantes shows in its
osteology an affinity both to Eurycea and to Plethodon. It
retains the eggs in the oviduct and gives birth to fully transformed
young. The same habit is found in the neotropical salamander
Oedipus structurally allied to Hydromantes. This would seem
to afford evidence that these genera are closely related. Many
tropical frogs pass their whole lives on land. There are oppor-
tunities for laying their eggs in water but the dominant groups
are those which have given up this primitive habit. Similarly,
Oedipus, which has freed itself from the necessity of returning
to water during the breeding season, represents a highly successful
stock. From the data available, it cannot be determined whether
Oedipus evolved from Plethodon or from Eurycea. At least we
may conclude that the ovo viviparity of Hydromantes and Oedipus
is further evidence of the close affinity of these two genera.

Salientia. — Turning to the frogs and toads, there are far more
genera to consider and their life histories are less known than
those of urodeles. Still, there is abundant evidence that their
mode of life history has usually changed gradually in phylogeny
and that a specialized method of caring for the young may be
common to many related species and even to several allied
genera. The recognition of this fact has helped greatly in

THE BIOLOGY OF THE AMPHIBIA

elucidating the relationships of various genera. For example,

Protopipa and Pipa are the
only frogs which carry their
eggs in individual dermal
chambers on the back of the
female parent and are un-
doubtedly closely allied.
Similarly, Phyllobates and
Dendrobates, which until
recently were placed in
separate families, are the
only genera which transport
their tadpoles on the back
of the male parent to
streams where they com-
plete their metamorphosis.
The South American tree
frogs, Cryptobatrachus,
Hemiphractus, Gastrotheca,
and Amphignathodon, have
been variously relegated by
herpetologists. Since they
are the only frogs which
carry their eggs in a single
mass on their backs (Fig.
20), whether or not this
mass is exposed or covered
by a fold of skin forming a
veritable sac, it appears
probable that they are
closely allied. This conclu-
sion is supported by the fact
that all the larvae have
distinctive bell-shaped gills
(Fig. 21 B-C). Many other
frogs lay their eggs out of
water and yet the larvae of
none of them have bell-
shaped gills.

Many frogs and toads
lay their eggs in the water and the polliwogs which emerge

Fig. 20. — The evolution of the dorsal
brood pouch of the Hylidae. A.
Gastrotheca marsupiata, the purse-like
brood pouch cut open on the side to
show the eggs within. B. Gastrotheca
pygmaea, female with the eggs removed
from the widely open brood pouch. C.
Cryptobatrachus evansi, female with eggs.

THE MODE OF LIFE HISTORY

may have distinctive characters of value to the systematist
in defining relationships. Some tadpoles may have narrow

Fig. 21. — Larval respiratory organs of some neotropical frogs. A. Eleu-
therodactylus inoptatus. B. Cryptobatrachus evansi. C. Gastrotheca marsupiata.
D. Hyla rosenbergi.

tail fins which permit them merely to wriggle along over
the bottom of the pond. Others may have broad fins and

THE BIOLOGY OF THE AMPHIBIA

well developed lungs, the latter functioning primarily as
hydrostatic organs. Such tadpoles, as for example those of
Hyla versicolor, are usually graceful swimmers. The characters
which these tadpoles exhibit are of importance in defining the
species. A synopsis of the tadpoles of the United States has been
given by Wright (1929), those of California by Storer (1925).
The tadpoles of many exotic species have also been described
(see bibliography in Noble, 1927). In the present summary,
reference may be made to only the more extreme modifications,
especially to those which have been employed as indicators
of the course of phylogeny.

Brevicipitidae. — The narrow-mouth toads, the Brevicipitidae,
include the most specialized of all the Salientia. Some are
narrow-snouted, burrowing types and others are broad-headed,
arboreal species. Nevertheless, all of their larvae, whether they
are hatched in the open ponds of our western prairies or between
the leaves of banana plants in the mountains of East Africa,
have the same distinctive characters (Fig. 22C). The only
exceptions are found among those forms which lay large-yolked
eggs hatching directly into frogs and among certain South African
brevicipitids which may possibly have evolved separately from
some ranid stock. This characteristic brevicipitid tadpole is
devoid of the usual horny teeth of the Rana polliwogs. It
lacks the suprarostral cartilage which supports the upper jaw
of most tadpoles, and the lower lip carries a series of folds which
in some species may be protruded considerably beyond the mouth
(Fig. 222?). The external nares do not break through until late
in larval life; the spiracle is median, unlike that of all other tad-
poles of the more advanced families of Salientia, with a single
possible exception. Apparently the toes as they develop are
always webbed, although this webbing may be entirely lost at
metamorphosis. The eggs, when laid free in ponds, are usually
equipped with a ridge on the outer capsule and the egg itself
lies eccentrically in the upper half of the egg capsule. Such
eggs have been described for Gastrophryne of America, Kalo-
phrynus of the Philippines, and Kaloula of Asia. Hence, it is
possible that they will be found throughout other genera of the
family which lay floating eggs, although they have not been
recorded elsewhere.

Various brevicipitids produce large eggs which develop directly
into frogs without passing through the tadpole stage. These

THE MODE OF LIFE HISTORY

Fig. 22. — Tadpole mouths. The shape is frequently correlated either with
the type of habitat or with the method of feeding. The umbrella mouth (B)
characterizes surface film feeders, while mountain-brook forms (D) frequently
possess large suctorial lips. Cannibalistic tadpoles (E) have strong mandibles
and sometimes broad lips. Some species, notably the Brevicipitidae (C), undergo
very little modification in spite of radically different feeding habits. A. Rana
alticola. B. Microhyla heymonsi. C. Gastrophryne carolinensis . D. Ascaphus
truei. E. Ceralophrys dorsaia.

THE BIOLOGY OF THE AMPHIBIA

are deposited on land, although there is one record of such eggs
being laid in water. This case was probably due to a flooding
of a stream near which the eggs had been laid. There are several
records of large-yolked eggs being able to develop in the water
after the egg capsules have been removed, but no attempt to
raise such eggs without removing these egg capsules has been
successful. Apparently these large eggs which go through a
rapid development require much more oxygen than they can
obtain in the water while enclosed by the egg capsules. How
greatly these large-yolked eggs of the brevicipitids differ from
similar eggs of other families is not entirely clear, for only a few
forms have been described in detail. Differences exist; for
example, the mucilaginous cord of Mantophryne is not found
in the bufonid Eleutherodactylus which also hatches fully formed
from the egg.

The Brevicipitidae have evolved from Ranidae and possibly
represent a polyphyletic assemblage, for the South African
genera, Hemisus, Cacosternum, and Anhydrophryne lack the
distinctive tadpoles of other Brevicipitidae. In the case of the
two latter genera it was possible to trace in their anatomy their
origin from the ranids in South Africa (Noble, 1926), but in the
case of Hemisus, the relationships are less clear. Hemisus is
one of the most characteristic burrowing toads of Africa. The
eggs are laid in burrows (Wager, 1929) and the tadpoles which
eventually escape into the water have peculiar sensory filaments
attached to the lower lip (Bles, 1907).

Ranidae. — The Ranidae represent a large, cosmopolitan family
of frogs. Their tadpoles exhibit various modifications, some
of the more peculiar being common to natural groups of species.
For example, the tadpoles of all species of Staurois are char-
acterized by an adhesive disc on the ventral surface behind the
mouth (Fig. 23). This permits the tadpoles to hold tightly to
rocks in the mountain torrents of southeastern Asia. The disc
was evolved out of the musculature and the abdominal integu-
ment of Rana tadpoles but few intermediate stages in the genesis
of the structure exist today (Noble, 1929 a). A second ranid
modification is found in the Philippine Cornufer. C. guentheri lays
large eggs which hatch directly into froglets. These are provided
with a series of pronounced folds along each side of the body.
A similar modification is found in the young Discodeles opisthodon
which also hatches fully formed. In the latter species the folds

THE MODE OF LIFE HISTORY

were described as respiratory structures but histological examina-
tion has shown that they are merely folds of the body wall pro-
duced by the rapid absorption of the yolk. This, apparently,
is a very trivial feature in the organization of these young frogs;
nevertheless, it occurs only in these closely related species.

Fig. 23. — Suctorial disc of a mountain-brook tadpole. A. Tadpole of Staurois
ricketti as seen from the ventral surface. B. The disc dissected free and viewed
from its dorsal aspect. Br. Sac, branchial sac; Cent.Prom., central prominence;
Fr.Ar., friction area; Fr.Rm., free rim; Jr., infrarostrale; Md., mandibulare;
M.D.M., M. diaphragmatobranchialis medialis; M.D.Prec, M. diaphragmato-
prfficordialis ; M.R.A., M. rectus abdominis; M. Sub. Br., M. subbranchialis;
Pericard., ligamentous posterior wall of pericardium, cut edge; Pois.GL, poison
gland; S.Hy.Lig., subhyoid ligament; S.Mx.Lig., submaxillary ligament; Spir.,
spiracle; S.Qu.Lig., subquadrate ligament; Sr., suprarostrale; Sub.Br.Prom.,
subbranchial prominence; Sub.Hy.Fol., fold over M. subhyoideus; Sub. Hy. Prom.,
subhyoid prominence; Sub.Mx.Prom., submaxillary prominence.

The tadpoles of the numerous species of Rana exhibit few
modifications. Those which live in swift waters resemble the
mountain-brook larvae of salamanders in lacking body fins and
in having the tail fins greatly reduced (Fig. 22 A). Unlike
salamanders their lips are frequently enlarged and assist them in
adhering to rocks (Fig. 23). In many of these species the number
of tooth rows is correspondingly increased. Some of the Indian
species of Rana, while enlarging their lips, tend to lose their tooth

THE BIOLOGY OF THE AMPHIBIA

rows. Where the latter are increased in number, as in Rana
boylii boylii of the western United States and in various Indian
species of Rana, this cannot be taken as evidence of relationship
between the forms but merely of parallel evolution. In many
other groups of frogs, as, for example, in the hylas of Haiti or of
Central America, closely related species may show marked differ-
ences in the size of the mouth and in the number of tooth rows.
Such differences are usually correlated with the rapidity of the
current in which the tadpoles live, the species with larger mouths
and most teeth occurring in the swiftest water. There is, how-
ever, an individual and an age variation in the number of rows
which may make the identification of forms difficult (Scott-
Biraben and Fernandez-Marcinowski, 1921).

One or two oriental species of Rana and another from South
Africa (Rose, 1929) have been reported to lay their eggs out of
water on leaves or stones or in the mud, but these egg masses
are unmodified and the larvae which escape soon make their way
into the water. The habit of laying eggs out of water is found,
however, in other ranids, as, for example, in one South African
species of Phrynobatrachus. Since other species of the genus
lay floating eggs, Wager (1930) considered this habit evidence
for retaining the species in a separate genus Natalobatrachus.
The habit finds a close parallel in certain neotropical tree frogs
of a very different family, to be discussed below.

Polypedatidae. — The Polypedatidae are Old World tree frogs
which have evolved from ranids and they have taken up the
habit of laying the eggs out of water and further elaborated it.
The most primitive genus is the well known Asiatic East Indian
genus, Rhacophorus or Polypedates. The vast majority of
the species in the genus lay their eggs over or near water and beat
the egg mass with their hind legs into a foam. This procedure
beats air into the developing spawn, an important feature, since
the outer surface of the foamy "nest" soon dries forming a
resistant crust to the nest. The central part of the nest liquefies
as the tadpoles develop and the latter are soon freed to take up a
life in the water. The older tadpole usually has a broad tail fin
which extends forward along the back. Two species of the
genus have succeeded in increasing the yolk content of the eggs
and these are no longer beaten into a foam. These large eggs
are probably hatched directly into frogs but observations on this
point are incomplete. In the Bufonidae the habit of making a

THE MODE OF LIFE HISTORY 67

foam nest has been evolved independently but here the eggs are
laid in contact with or very near the water, while the tadpoles
never develop the larval characters of Polypedates. It is,
nevertheless, interesting that the habit of making foam nests
should have independently evolved in these two unrelated groups.

All the genera which show anatomical evidence of having
evolved directly from Polypedates have retained the same
mode of life history. Several species living in the same region
as Polypedates have been found to have the same habit, while
the African Chiromantis which is another derivative of Poly-
pedates has exactly the same way of caring for its eggs. The
life histories of African frogs related to Chiromantis are incom-
pletely known, but some such as Hyperolius, lay their eggs in
small clusters in the water (Rose, 1929) and here it is apparent
that the spawn-beating habit has been given up. Kassina
senegalensis is closely related to Hyperolius and has also given
up the egg-beating habit. Its eggs are small, only 1.5 mm.
without the capsules, pigmented, and laid singly or in pairs in the
water (Power, 1926). The mature tadpoles are of the back-
finned Polypedates type; the tooth rows, however, are more
reduced than in most species of the ancestral group. Although
Kassina and Hyperolius have succeeded in giving up their spawn-
beating habit, they still show in the tadpole form some evidence
of their origin. Further, the tadpole of Kassina develops a rigid
convex upper lip and a pair of horny plates obliquely arranged
in the angle of the mouth. Such structures are known only
in the tadpoles of Hylambates, a genus more closely related to
Kassina than to Hyperolius. Until recently Hylambates was
confused with another genus of polypedatids, Leptopelis. Since
the tadpoles of one South African species lack these plates
(Wager, 1930), it remains to be discovered if the genera Leptopelis
and Hylambates may be distinguished on the basis of different
larval modifications.

Hylidae.— The typical tree frogs, Hylidae, show no close
relationship to the Polypedatidae ; they have evolved from
bufonids, not ranids. As already indicated, one group of hylids,
which may be defined as Gastrothecinae, carries its eggs on the
back of the female, some exposed and others enclosed in a sac.
None of the other hylids shows any indication of this mode of
life history, nor are the larvae equipped with bell-shaped gills
which are found throughout the first subfamily. All of the latter

THE BIOLOGY OF THE AMPHIBIA

hylids lay their eggs in pools. Some, such as Hyla rosenbergi
and the closely related H. faber, build basins of mud either near
the edge of pools or in the bed of the pool itself. In the case
of the former species, at least, the male does all of the building
and he attracts the female to the basin with his voice, after the
walls are constructed. The tadpoles (H. rosenbergi at least)
which are developed within these muddy cups have enormous
pinnate gills which adhere to the surface film of the basins.
Similar gills have been described in Leptodactylus ocellatus which
is not closely related to H. rosenbergi. The former lays its eggs
in a foamy mass similar to other species of the genus Lepto-
dactylus and no mud basin is constructed. The gills, while
long (Fig. 21Z>), have the simple structure of the gills of other
species of Hyla and hence their hypertrophy, which seems to be
correlated with the poor oxygen supply of the basins, has brought
no radical change in their structure. Other tree frogs of the
genus Hyla lay their eggs in small basins of water existing in
nature. For example, the tree frogs of Jamaica lay their eggs
in water between the leaves of bromeliads. In such a habit we
apparently have the beginning of the basin-building habit of
Hyla rosenbergi and H. faber. The two latter species are more
closely related to one another than to any other tree frog whose
life history is known and they have similar modes of nest building
different from that of any other frog.

Within the genus Hyla, other closely related groups of species
have similar habits. All the hylas of Jamaica lay their eggs in
bromeliads and the larvae are modified for living in close con-
finement. The larval tooth rows have been reduced and also
the larval gills. Hence, these tadpoles apparently secure most
of their oxygen directly from the atmosphere. The food supply
in these situations is limited and the tadpoles have developed
the habit of eating the eggs of their own or related species laid
in the same situation. It is interesting that brevicipitid toads
of the genus Hoplophryne should have adopted a somewhat
similar habit of laying their eggs in or near basins of water. They
also exhibit a reduction of the gills and both possess a powerful
development of the jaws (Noble, 1929a). Apparently the latter
modification assists them in cutting through the capsules of the
eggs they eat. In spite of the parallelism of habit and diet,
the tadpoles of each group show definite evidence of their group
relationship. Those of Hoplophryne have the characteristic

THE MODE OF LIFE HISTORY

brevicipitid features described above, while hylas resemble one
another in the reduction of the larval tooth rows (Fig. 24).

Other species of Hyla have adopted still other modes of life
history. Hyla uranochroa,
for example, apparently
lays its eggs out of water
on leaves and the tadpoles
which finally make their
way into the water are
forced to live in the rapid
streams where they find
themselves. This tree frog
has a red iris similar to
many species of the genus
Phyllomedusa. The latter
is merely a Hyla which
has undergone various
reductions in the length of
certain digits. All species
of Phyllomedusa, as far
as is known, lay their eggs
over water. They do not
beat this egg mass into
foam as in the case of Poly-
pedates, but in some species
the parents may fold the
leaves together over the
mass of eggs. The tad-
poles which hatch have a
broad back fin similar to
Hyla versicolor. One spe-
cies of the genus has been
recorded to have its mouth
produced into a funnel
which apparently assists it
in surface feeding. A sim-
ilar umbrella mouth has

Fig. 24. — The modification of the mouth
parts of the tadpoles of Jamaican tree frogs:
A. Hyla lichenata. B. Hyla brunnea. C.
Hyla marianae. D. Hyla wilderi.

been recorded in the brevicipitids, Microhyla achatina and M. hey-
monsii tadpoles, as well as in many species of the pelobatid Mega-
lophrys and in one species of the brachycephalid Phyllobates (Fig.
22B). Some of these species live in mountain brooks and others

THE BIOLOGY OF THE AMPHIBIA

in ponds. The funnels differ in detailed form but in all cases
they are umbrella-like extensions of one or both of the larval lips.
No doubt the funnels assist some species, if not all, in increasing
the efficiency of surface feeding, but when one considers the
sporadic occurrence of these enlarged lips in totally unrelated
groups of frogs, it becomes clear that they do not afford a good
evidence of relationship. Since tadpoles with and without
enlarged mouths are sometimes found together in the same ponds,
it does not seem that the presence of these enlargements is a
matter of life or death in the economy of these species. It would
be interesting to know whether the tadpoles with the large
mouths invariably feed on a different kind of food from that on
which the others do. In the adult frogs there is no specialization
of food habits permitting two closely related species to live in the
same region. Possibly competition is avoided in these tadpoles
by the very different mouths of the larvae.

Brachycephalidae. — A second family of predominantly neo-
tropical Salientia is the Brachycephalidae. Like the Hylidae
they also evolved from toothed bufonids but they specialized
in terrestrial life. As mentioned above, Phyllobates and Dendro-
bates are closely related and the males of both genera carry their
tadpoles on their backs, at least while transporting them to the
pools from the site where the eggs were laid. The habit is
known from a series of species, some living at high altitudes
in the Andes and others at sea level in tropical jungles. The
habit forced on the group by phylogeny was found useful in
many different kinds of situations. How the habit actually
developed is not known since the life history of the genera imme-
diately ancestral to Phyllobates has not yet been worked out.

A second group of Brachycephalidae seems to have had an
independent origin from bufonid ancestors. This group includes
the diminutive frogs of the genus Sminthillus. Their anatomy
suggests that they have evolved directly from Syrrhophus or its
close relative Eleutherodactylus. Like the latter genus, Smin-
thillus limbatus of Cuba lays large eggs on land. Apparently
these undergo the usual development of Eleutherodactylus.
Sminthillus is very small, and each female, as far as known, lays
only a single egg, while the many species of Eleutherodactylus,
whose life histories are known, lay considerably more. Such a
reduction in egg number is apparently correlated with the small
size of the species.

THE MODE OF LIFE HISTORY

There is one genus of Brachycephalidae, Rhinoderma (Fig. 25),
which has attracted attention for many years because the male
carries the eggs in his vocal pouch until they hatch as fully formed
frogs. The tadpoles during this period have typical larval
mouth parts, although these remain uncornified. The papillae
about the mouth resemble
more closely those of
the bufonid Paludicola, as
described by Fernandez
(1927), than those of the
brachycephalid Dendrophry-
niscus stelzneri, described by
the same author. No inter-
mediate stages between this
remarkable habit of carrying
eggs in the vocal pouch and
the more usual habit of
laying eggs in the water
are known. Many fish are
" mouth breeders," that is,
they carry their eggs for
various periods during de-
velopment in the buccal
cavity, but no species of
frog has this habit, although
an African form was in-
correctly described as doing
so.

The retention of larval structures in situations where they
cannot function finds a parallel to Rhinoderma in other groups.
The South African Arthroleptella lightfooti develops a branchial
sac devoid of a spiracle, although the species undergoes its
entire development on land and is unable to swim when placed
in the water. Again, the African Breviceps parvus undergoes
even a more direct development from egg to frog but nevertheless
possesses a branchial sac within which the forelimbs develop
(de Villiers, 1929). Possibly these or other larval retentions may
afford a clue to the ancestry of these groups, but so little is known
concerning the larvae of the Brachycephalidae that the phylo-
genetic significance of the larval teeth of Rhinoderma cannot be
stated.

Fig. 25. — A dissection of the vocal
pouch of Rhinoderma darwinii showing
several partly metamorphosed larvae.
The young undergo their larval develop-
ment within the vocal sac of the male.
V.S., vocal sac; M.L., metamorphosing
larva.

THE BIOLOGY OF THE AMPHIBIA

Bufonidae. — Mention has been made of the direct development
of Eleutherodactylus. This genus belongs to the large group of
tooth-bearing toads formerly called "Leptodactylidae." A
study of the anatomy of the toothed and the toothless toads in
various parts of the world disclosed that many genera in different
parts of the world had independently lost their teeth. Placing
all the toothless species by themselves in a separate family made
a very unnatural assemblage. As indicated above, life history
data supported this contention, for various groups of toothless
and tooth-bearing toads were found to have the same life-history.
The habit of Eupemphix of beating its egg mass into a foam which
it had laid in or near small pools of water was found not only
in the toothed genus Paludicola, immediately ancestral to Eupem-
phix, but also in the whole series of species referred to several
genera. These include the dominant group of South American
frogs, namely Leptodactylus. Some species of the latter genus
may be as large as the American Bullfrog and others only a
little larger than a Spring Peeper, Hyla crucifer, and yet they all
lay their eggs in a foamy mass. A parallel occurs in some species
of Polypedates, but here the egg mass is not laid in contact with
water, and the larvae, as they develop, are differently modified.
While enclosed within the foamy mass, the larvae of Lepto-
dactylus, Paludicola, and Eupemphix have very slim bodies
which may be of assistance in their efforts to break through their
slimy nests to the adjacent water. Differences appear in the
various species; for example, in the length of the gills. Neverthe-
less, there is a general agreement of nest form and larval habitus
which runs through the whole group.

The only exception known at the present time to foam nest
building as characteristic of all species of Leptodactylus and its
allies is found in a species at present referred to the genus Pleuro-
dema. Fernandez (1927) reported this species to lay its eggs in
regular masses, but since the eggs were not collected by Fer-
nandez, there is some possibility of error. The evidence as
given would indicate that a life-history mode may remain con-
stant throughout a great many related species and genera and
suddenly, within a single genus, change to a totally new type.
Within many genera egg size may increase and species with the
largest eggs will develop into frogs instead of going through the
tadpole stage. But there is very little evidence of radical

THE MODE OF LIFE HISTORY

changes in the mode of life history among closely related species
which pass through the tadpole stage.

Although egg size may shift within closely related species, it is
interesting that it frequently remains constant throughout a
large series of forms. For example, all species of Eleuthero-
dactylus apparently lay their eggs on land; the eggs are devoid
of peduncles and are not beaten into a foam. The embryos as
they develop may or may not be provided with external gills.
They are all equipped with a broad, thin tail which functions as a
respiratory organ. No other species of frogs laying eggs on
land is equipped with this respiratory tail at the time they are
enclosed within the egg capsule, except certain East Indian
brevicipitids. In these brevicipitids, the eggs are laid in the
form of a rosary and the tadpoles which develop are not known
to have the powerful egg teeth of Eleutherodactylus (Fig. 26).

Fig. 26. — The egg teeth of two frogs. A. Eleutherodactylus abbotti. B. E.

inoptatus.

The egg teeth in Eleutherodactylus usually have the shape of a
pair of bull's horns which help the little frog when mature to
escape from the capsule. There are, thus, apparently important
details of development to distinguish the mode of life history
found in Eleutherodactylus from that in other frogs laying eggs
on land. Again, these differences are not sufficiently known in
any number of species for us to be sure which are the most
diagnostic.

That the form of the egg capsule really may be an important
character uninfluenced by environmental factors is well shown
in the case of the common toad. Species of Bufo are found
throughout the greater part of the world. Species laying their
eggs in deserts, in jungles, or on mountain tops all produce the
same characteristic string of eggs found in our common Bufo.
There is, to be sure, one exception from the East Indies which
has not been accounted for (Noble, 1927) and also the instance
of the Oak Toad of Florida which sometimes lays its eggs in

THE BIOLOGY OF THE AMPHIBIA

small rods instead of strings (Wright and Wright, 1924). The
latter case may be accounted for by assuming the modification
to be due to the extremely small size of the adult. Since the
Bufo stock of South America must have been separated from
that in South Africa for many thousands of years, and both
must have migrated across jungle and plain to reach their present-
day ranges, .it is remarkable that both are able to succeed so
well with this simple mode of egg laying. It is probable that
factors other than the mode of life history have been chiefly
responsible for the toad's success; nevertheless, the method of
laying the eggs in strings has not been detrimental to the species
under these various environmental conditions, or the stock would
have died out.

Ovo viviparous Bufonids. — Within a single family there may be
several modes of life history. In the Plethodontidae discussed
above, some species lay their eggs in water, others on land, and
still others retain them in the oviducts until fully formed young
emerge. Similarly in the Bufonidae different ways of propaga-
tion may occur. There is one group of African frogs, referred
to the genus Nectophrynoides, the two species of which are
structurally very different. Until recently they have been kept
in separate genera, but both give birth to their young alive. No
copulatory organs have been described, and how the spermatozoa
are transmitted to the oviduct is not known. The embryos as
they develop have very slim tails which no doubt are of little
use as locomotory organs. The tails are well vascularized, how-
ever, and greatly elongated. This seems an adaptation to secur-
ing oxygen from the vascular uterine wall. The number of
larvae within a single uterus of N. vivipara is often over a hundred,
and the long tails apparently function as so many pipe lines
bringing oxygen to the larvae kept away from the uterine wall
by the bodies of their brothers and sisters. As in the case of
Rhinoderma, the stages by which this ovoviviparity in Necto-
phrynoides was secured are unknown. In fact the many peculiar
life histories of tropical frogs are known so fragmentarily that
we are able to compare only the general mode of life history rather
than the details of development. Where these details are known,
however, they sometimes exhibit marked adaptations which
have no especial phylogenetic significance. Examples may be
found among the tadpoles of Ceratophrys, two species of which
have large mouths and many tooth rows as an adaptation toward

THE MODE OF LIFE HISTORY

a cannibalistic diet. Mountain-brook tadpoles may have large
mouths which assist them in holding on to rocks in midstream.
In these cases tadpoles with few, and others with many tooth
rows may be closely related.

The mode of life history thus forms a guide rather than an
infallible proof of the relationship of frog or toad. Where the
affinities of genera or species are in doubt the mode of life history
frequently gives an important clue. For example, the torrent
frogs of Rio de Janeiro, called Hylodes petropolitanus and
Borborocoetes miliarus, have peculiarly flattened tadpoles adapted
for gliding over wet stones or trickles on the edge of the torrents.
These tadpoles are so different from any other species that there
can be little doubt as to the close affinity of the two forms.
More recently, Lutz (1928, 1929) has shown that the tadpoles
of two species of Cycloramphus resemble these flat tadpoles
closely but are more elongate and may have different mouth
parts and spiracles. The eggs of all these species are apparently
laid out of water among the rocks and the tadpoles are more
truly amphibian, that is, both aquatic and terrestrial, than those
of any other frog of South America. This habit and habitus
of the tadpoles is not an ontogenetic modification produced by a
peculiar environment. In the same mountain torrents there
are various species of Elosia which frequent the rocks but produce
large tadpoles of the usual torrent type. The edges of mountain
torrents are attractive to many species of frogs but each holds
to its own mode of life history which is primarily dependent on
the heredity of the species. In the present instance the mode of
life history would seem to be a better clue to relationships of the
species than many of the so-called generic characters. In other
words, marked changes in the dilation of the digits, the webbing
between the toes, and various other external characters of the
adults have occurred, while the mode of life history remained
the same.

Primitive Salientia. — Finally, mention should be made of the
most primitive families of frogs and toads — Liopelmidae, Dis-
coglossidae, Pipidae, and Pelobatidae. With the exception of
the last, there are few genera to consider and these are widely
separated geographically. No doubt the first three represent
ancient stocks and hence the mode of life history is often strik-
ingly different within each family. Nevertheless, all are charac-
terized by the pelvic embrace of the male during breeding,

76 THE BIOLOGY OF THE AMPHIBIA

while most higher frogs and toads practice the pectoral amplexus,
although occasionally the amplexus may be pelvic in very
stout species. The observations of Fletcher (1889), that the
Australian Limnodynastes, Hyperolia, Pseudophryne, and Crinia
employ a pelvic embrace is of interest, for it strongly suggests
that these toads are more primitive than other bufonids. Nearly
all tadpoles of liopelmids, discoglossids, and pelobatids exhibit
smooth edges to their larval teeth, which frequently appear in
duplex rows. A doubling of the sets of teeth within each tooth
row appears extremely rarely among higher forms, and the tad-
pole teeth of the latter are usually serrated. Where specializa-
tions occur in the life history, these are unique. Mention has
been made of Protopipa and Pipa as the only two frogs which
carry their eggs in separate pockets on their back. Mention
has been made also of Ascaphus (Fig. 22D), whose tadpoles live
in the mountain torrents of the West. The arrangement of the
tooth rows of Ascaphus is unique among the Salientia. While
the species of these primitive genera are too few to trace out
their progressive evolution in their mode of life history, never-
theless, in general they support the view that the mode of life
history is usually of considerable phylogenetic significance.

Gymnophiona. — The caecilians, which have been found to be
primitive in many features of their anatomy, possess large-
yolked eggs. Some of these are laid on land as in Ichthyophis,
and the female guards them until the larvae hatch and take up a
life in the water. Others skip over the aquatic larval stage and
a few have specialized external gills. One genus, Typhlonectes,
is ovoviviparous. No caecilian has a less specialized life history
than that of the more primitive genera Ichthyophis and Rhina-
trema. The life histories of Ichthyophis, Hypogeophis, and
Typhlonectes show a gradual specialization of life history
accompanying a specialization in adult structure.

The Primitive Type. — Lastly, it should be emphasized that
there is no reason for assuming that the small eggs of Rana are
primitive. The branchiosaur ancestors of frogs and urodeles
arose from labyrinthodonts and these ancient Amphibia were
almost indistinguishable from some cotylosaur reptiles. Possibly
these labyrinthodonts had not developed the amnion, allantois,
or calcareous egg membranes of modern reptiles, but it is not
improbable that the eggs were well provided with yolk. Another
inheritance from fish ancestors was the gelatinous egg capsules

THE MODE OF LIFE HISTORY

which serve not only as a protective cover but also as a regulator
of osmotic conditions in the egg. In species exposing their eggs
to the sun the capsules have the additional function of conserving
heat by checking radiation.

References

Bishop, S. C, 1919: Notes on the habits and development of the four-toed

salamander, Hemidactylium scutatum (Schlegel), N. Y. State Mus.

Bull., 219-220, 251-282.
Bles, E. J., 1907: "Notes on anuran development; Paludicola, Hemisus,

and Phyllomedusa," The Work of John Samuel Budgett, Cambridge,

443-458, pis. XXII-XXVII.
Brimley, C. S., 1923: The dwarf salamander at Raleigh, N. C, Copeia,

N. Y., No. 120, 81-83.
Despax, Raymond, 1923: Contribution a F etude anatomique et biologique

des Batraciens urodeles du groupe des Euproctes et specialement de

l'Euprocte des Pyrenees, Theses pour Docteur Sci. Nat. Toulouse, Ser.

A, No. 929.

de Villiers, C. G. S., 1929: Some features of the early development of

Breviceps, Ann. Transvaal Mus., XIII, 142-151.
Escher, Konrad, 1925: Das Verhalten der Seitenorgane der Wirbeltiere

und ihrer Nerven beim Ubergang zum Landleben, Acta Zool.f VI,

307-419.

Fernandez, K., 1927: Sobre la biologia y reproduccion de batracios argen-
tinos (Segunda parte), Bol. Acad. Nac. Cien. Cordoba, XXIX, 271-328,
4 pis.

Fletcher, J. J., 1889: Observation on the oviposition and habits of certain

Australian Batrachia, Proc. Linn. Soc. N. S. Wales (2), IV, 357-390.
Ltjtz, A., 1928: Biologie et metamorphose des Batraciens du genre Cyclor-

hamphus, Compt. rend. Soc. Biol, XCVIII, 640.
, 1929: Taxonomy and biology of the genus Cyclorhamphus, Mem.

Inst. Oswaldo Cruz, XXII, 16-25, 5 pis.
Moesel, J., 1918: Thesis: a study of the Caudata of the Cayuga Lake

Basin, Cornell Univ. MS.
Noble, G. K., 1926: The importance of larval characters in the classification ,

of South African Salientia, Amer. Mus. Novit., No. 237.
, 1927: The value of life-history data in the study of the evolution of.

the Amphibia, Ann. N. Y. Acad. Sci., XXX, 31-128, 1 pi.
— , 1929 : Further observations on the life history of the newt, Triturus ,

viridescens, Amer. Mus. Novit., No. 348.
, 1929a: The adaptive modifications of the arboreal tadpoles of

Hoplophryne and the torrent tadpoles of Staurois, Bull. Amer. Mus.

Nat. Hist., LVIIi, Art. VII, 291-334.
Power, J. H., 1926: Notes on the habits and life histories of certain little-
known Anura, with descriptions of the tadpoles, Trans. Roy. Soc. S.

Africa, XIII, 107-117, pis. VI-IX.
Power, J. H., and Walter Rose, 1929: Notes on the habits and life histories

of some Cape Peninsula Anura, Trans. Roy. Soc. S. Africa, XVII,

109-115, pi. V.

THE BIOLOGY OF THE AMPHIBIA

Rose, Walter, 1929: "Veld and Vlei: An account of South African frogs,
toads, lizards, snakes and tortoises," Cape Town.

Schmalhausen, I., 1917: On the extremities of Ranidens sibiricus Kessl,
Rev. Zool. Russe, II, 129-135.

Scott-Biraben, M. T., and K. Fernandez-Marcinowski, 1921: Variaciones
locales de caracteres especificos en larvas de anfibios, An. Soc. Cient.
Argentina, XCII, 129-142.
, Smith, Bertram G., 1912: The embryology of Cryptobranchus alleghen-
iensis, including comparisons with some other vertebrates; Part I,
Introduction: the history of the egg before cleavage, Jour. Morph.,
XXIII, 61-154; Part II, General embryonic and larval development,
with special reference to external features, Jour. Morph., XXIII,
455-579, 10 pis.

Storer, T. I., 1925: A synopsis of the Amphibia of California, Univ. Cal.

Pub. Zool, XXVII, 1-342, 18 pis.
Wager, Vincent A., 1929: The breeding habits and life histories of some

of the Transvaal Amphibia, II, Trans. Roy. Soc. S. Africa, XVII,

125-135, 5 pis.

■ , 1930: The breeding habits and life histories of two rare South

African Amphibia, I, Hylambates natalensis, A. Smith; II, Nataloba-
trachus bonebergi, Hewitt & Methuen, Trans. Roy. Soc. S. Africa,
XIX, 79-92, 5 pis.

Wright, A. H., 1929: Synopsis and description of North American tadpoles,

Proc. U. S. Nat. Mus., LXXIV, Art. 11, 1-70, 9 pis.
Wright, A. H., and A. A. Wright, 1924: A key to the eggs of the Salientia

east of the Mississippi River, Amer. Naturalist, LVIII, 375-381.
Wunderer, Hans, 1910: Die Entwicklung der ausseren Korperform des

Alpensalamanders (Salamandra atra Laur), Zooi. Jahrb. Anat. Abt.,

XXIX, 367-414, pis. XXV-XXXIII.

CHAPTER IV

SPECIATION AND ADAPTATION

It is self-evident that Amphibia are more or less adapted to
their environment. Burrowing toads are equipped with tarsal
"spades" (Fig. 27), pond salamanders with lateral line organs,
arboreal frogs with large adhesive discs. If Amphibia were not
in more or less harmonious relation with the habitats in which

Fig. 27. — A fossorial adaptation. Skeleton of the right foot of Rhinophrynus
dorsalis, mesial aspect. The prehallux and first digit are modified for digging.
F., fibula; Fe., fibulare; Aft., metatarsal of first digit; Pr.H., prehallux; T., tibia;
Tar., fused tarsalia; Te., tibiale.

the different species spend the greater part of their lives, be that
aquatic, terrestrial, or arboreal, they would eventually succumb.
Each of the chapters devoted to the structure of Amphibia dis-
cusses some illustration of the adjustment or modification of
organs and tissues as correlated with the particular needs of the
organism. Amphibia, like most other organisms, when under
the stress of unusual environmental conditions, can modify
during development the full expression of various structures.
But the alterations of development will explain very few of the
extraordinary adaptations found in the group. In considering
the latter, some account must be given of the mechanism by which
both species and their distinctive characters come into existence.
Emphasis will be laid on the origins of adaptations rather than on
a detailed description of them.

THE BIOLOGY OF THE AMPHIBIA

Species Defined. — Species are groups of individuals having
one or more characters in common which distinguish them from
related groups of individuals. Groups exhibiting characters in
common but intergrading with those of a closely related group
are usually defined as subspecies and a third name is added
to the species name. For example, Desmognathus fuscus caro-
linensis is the subspecies of the common Dusky Salamander
D. fuscus. Species may embrace several subspecies but they
may also include many variants, incipient species, and some-
times " sports." The relation of these various infraspecific
categories to species is still a controversial matter in spite of the
efforts of many investigators (cf. Cuenot, 1921; Morgan, 1923;
Robson, 1928; Rensch, 1929). The Amphibia have contributed
little to an experimental analysis of the problem, but various
facts concerning their distribution and phylogeny have been
used to bolster up now one view, now the other. Since it has
been the systematist who has first defined and has been most
concerned with species as steps in evolution, some reference
may be made to the kind of data which have been employed by
the systematist when considering species origin.

Variation. — The individuals of any one species frequently
vary greatly among themselves. Variation of color is well known
in the Cricket Frog, Acris, and in the Leopard Frog, Rana pipiens.
Variation has been described in toe number in Hynobius, verte-
brae number in Dendrobates, and egg size in some species of
Rana. Similar differences when fixed have been used in defining
other groups of Amphibia. The toad, Bufo americanus, is not so
variable as many species of Salientia, but Kellicott (1907) found
many differences in the 13 characters he considered in a single
colony of the species. In various species of Salientia individuals
may appear with a conspicuous dorsal stripe, and as similar
stripes may be characteristic of other species but not those under
consideration, they have been considered sports or pronounced
mutations (Mertens, 1926). Darwin was familiar with such
differences, but he rejected them as a possible source of species
formation. He appealed to the small heritable variations found
in all species of animals as furnishing the material for species
production. Since Darwin's time, naturalists have greatly
increased the number of instances of species differing from others
merely by slight differences of color or form. On the other hand,
geneticists have demonstrated that these small differences are

SPECIATION AND ADAPTATION

also due to germinal mutations and that they arise and are
inherited in the same way as the large heritable changes or sports.
In brief, the systematist considers the same kind of data which
Darwin utilized, only more examples are available today
and much more is known of the way the characters are
inherited.

Hereditary Units. — All heritable differences distinguishing
species which have been adequately studied have been found to
be produced either by recombination of the genes (the hereditary
factors) upon crossing; by aberrations of the chromosomes, the
bearers of these hereditary factors; or by mutation, that is,
change in the individual genes. Most variation displayed by a
population of a single species in nature is usually due to recom-
bination of preexisting mutations. Because recombination occurs
so much more frequently than mutation, each individual is not the
final member of a single series but of converging lines of descent
which ramify throughout the entire specific group (Fisher, 1930).
Most wild species are heterozygous, that is, unlike in a number
of pairs of homologous genes derived from father and mother,
respectively. As a result, the effect of any one member of the
pair may be modified, and different grades of any one variation
may appear within a species. Such variation may appear to be
continuous, in striking contrast to the pronounced mutations
first studied in domesticated animals and plants. This has led
many naturalists to assume that speciation was continuous;
mutation, discontinuous. In every case where the material
has been subjected to adequate breeding tests, however, this
distinction was found to be non-existent. Large and small
heritable differences were found to have the same kind of chromo-
somal basis. Geneticists have shown that the greater the effect
of a single mutation, the more likely it is of being not viable.
Mutations which produce relatively slight changes are least
likely to be harmful and therefore most likely to be preserved by
natural selection. It is for this reason that the differences which
distinguish species of Amphibia are usually very slight. There is,
however, some evidence that mutations of some magnitude have
played a role in the evolution of the Amphibia.

Unfortunately for the present review, the genetic analysis has
not proceeded far enough to determine how many mutations
distinguish any one species of Amphibia from another. The
albino axolotl is known to differ from the normal colored phase

THE BIOLOGY OF THE AMPHIBIA

merely by a single Mendelian factor (Haecker, 1908), although
there appear to be various degrees of albinism in this species
which may be due to other genetic factors. Amphibia are slow-
breeding creatures and we may never know how many gene
mutations distinguish the axolotl from the other species of
Ambystoma. In the meantime, geneticists have brought to
light additional facts which give an explanation for the essential
requirements postulated by many naturalists for the origin of
species in nature.

Isolation in Species Formation. — It has long been recognized
that " without isolation no species" will be formed. Recent
investigations have emphasized that isolation alone is not so
effective as isolation plus change of environment (Grinnell, 1924 ;
Chapman, 1926). Random mating in a natural population of
any one species tends to distribute all the different genes
throughout the population. Since most mutations occur in only
one member of a pair of genes and are recessive (Morgan, 1926),
they cannot come to expression until they meet with other like
genes on crossing. Isolation encouraging inbreeding hastens
the appearance of the characters, and continued inbreeding tends
to change the isolated group into one which is homozygous for
these characters. Hence stocks isolated on islands, on mountain
tops, or in well-defined ecological niches soon exhibit and fix
characters which their wide ranging, freely interbreeding ances-
tral stocks fail to show. If in addition to this uncovering process
the isolated community is subjected to new environmental
conditions, the stock will be reduced to only relatively few indi-
viduals of those best fitted to survive. The uncovering will
proceed more quickly, and natural selection will presumably favor
individuals unlike those of the original stock. It is thus no wonder
that while some species of tree frog have a wide range in Central
America, each of the Greater Antilles has its own species. Nor
is it surprising that mountain ranges with their diverse topography,
whether in the Old or in the New World, usually have a greater
number of distinctive types of frogs and toads than the adjacent
low country of much greater area.

It may be noted, however, that continued isolation does not
improve the strain beyond a certain point. No change will
occur in this pure line until a mutation happens to occur in some
gene. Isolation favors the rapid purification of hidden strains
but has no influence on inducing new mutations.

SPECIATION AND ADAPTATION

It is frequently supposed that inbreeding within an isolated
community leads to a decrease of vigor. This does not always fol-
low. In a wide-ranging species individuals with dominant genes
having unfavorable effects are soon eliminated in the struggle to
live. Unfavorable recessive genes, on the other hand— those
which do not have any visible effects — may become widely
spread throughout the population. Inbreeding of a sample of
this population leads to the appearance of these effects, for the
inbred individuals tend to become homozygous for these genes.
Hence isolated communities of small size are usually less vigorous
than communities of a larger size which are frequently " mixing"
their germ plasm. If this small group is suddenly thrown into
competition with a wide-ranging group, it will usually succumb
because it is less vigorous due to its genetic constitution. It is
of course possible, however, that the pure line produced by isola-
tion and inbreeding would be more vigorous than a wide-ranging
stock due to the selection of certain favorable genes. The
chances, however, are very much against such a possibility in
nature.

Kinds of Isolation. — Multiplication is so rapid within any spe-
cies of animal that a balance of numbers is soon struck, depend-
ent on available food and other conditions limiting life in a
particular habitat. Competition is most keen between organisms
whose food and other requirements are most alike. Hence a
decided premium is placed on mutations which tend to throw
their owners out of competition with their near relatives. Genet-
icists have shown that a single gene mutation may affect many
organs of the body at one time and also influence physiological
processes of great importance in the life of the animal. As Mor-
gan (1923) has said, it is these physiological effects which have
played the most important role in evolution. In the first place,
they might tend to isolate the individuals possessing them as effec-
tively as a river barrier. It is chiefly physiological differences
which induce species to select different breeding sites or appear
at different seasons or take up an abode in different habitats.
In the second place, they might affect the reactions of one indi-
vidual to another or even induce infertility. Systematists have
not been concerned with the characters which have created the
species. For example, the Japanese tree frog, Polypedates
schlegelii, has a form arborea differing from the typical form in its
slightly more pointed snout and smaller size (Okada, 1928) but

THE BIOLOGY OF THE AMPHIBIA

it differs radically from the typical form in laying its eggs in
frothy masses on leaves over the water instead of in holes in the
banks of rice fields. The difference between the two forms is so
slight that they are not considered good species. Since the forms,
however, are apparently completely isolated during the breeding
season, the two " varieties" will continue to accumulate small
mutational differences until they become good species. Outside
the breeding season many species of frogs and salamanders may
occupy the same habitat. Robson (1928) in his review of species
formation failed to find isolation an important factor, apparently
because his data on the kinds of isolation were incomplete.
Geographic isolation is the most obvious but by no means the
only important kind of isolation which may occur. For example,
Plethodon cinereus and P. glutinosus are two common salamanders
of eastern United States. As shown by Shelford (1913), the
latter is more sensitive to dry air than the former and this would
explain why the latter is usually found in more moist situations
than the former. Further, P. cinereus lays its eggs in logs or
under stones in the woods, while P. glutinosus seeks a subterranean
retreat for egg laying. Lastly, the two species are of very dif-
ferent sizes and hence would not compete for the same food. If
a derived stock is thrown out of competition with the ancestral
group and cross-breeding is prevented due to morphological or
physiological change, the first step in the origin of a new species
has been made.

Not all closely related species are isolated, and some may be
thrown into direct competition. In such cases the factors per-
mitting survival may be complex. Recently Piersol (1929)
has found that Amby stoma jeffersonianum, although breeding in
the same ponds as A. maculatum, maintains the same relative
abundance from year to year in the Toronto region. The first
species breeds a little earlier than the second and a higher percent-
age of its eggs fail to develop. Piersol has shown that this loss is
due to the cold, which in some cases may prevent the sperm from
entering and in others may favor an abnormal polyspermy leading
to irregular changes and death. Further, low temperatures below
5°C. result in such a slowing of development that the egg materials
tend to stratify and the egg dies. These losses, however, are
compensated for by the cannibalistic tendencies of the larvae and
the earlier start they obtain in life. Piersol showed that when
the larvae of the two species were crowded and starved, the

SPEC I AT ION AND ADAPTATION

jeffersonianum larvae devoured the maculatum. If jeffersonianum
larvae were not so aggressive and voracious, maculatum would
soon replace jeffersonianum as a species, for it has inherited a
breeding season rhythm better fitted to the Toronto climate.

Not only the time of breeding but the duration of the breeding
season may be due to genetic factors. Witschi (1930) found that
two strains of Rana temporaria differed in the length of the breed-
ing season. When the rapid breeders were brought into the
laboratory, they deposited their eggs in 24 hours while the slow
breeders under the same conditions required a longer period.
Correlated with this difference in breeding rate was an inherited
difference in rate of sex differentiation. Further, the rapid
breeders came from regions with long winters and short though
relatively hot summers. Their breeding rhythm was adapted
to the habitat of the strain. No doubt natural selection had been
instrumental in localizing each strain in that region most suited
to its particular rhythm.

Space and Time in Evolution. — Species change with space and
time: with space because they meet new environments and this
permits new isolations and new selections, with time because any
one locality is undergoing a cyclic climatic change (Matthew,
1915) which will eventually alter both the physiography and
flora of the region. Since species usually avoid competition by
migrating into new territory, Jordan (1926) has postulated that
the nearest relative of any species is not likely to be found in the
same region, but in a neighboring one separated by a geographical
barrier. Since an active or passive migration is occurring at all
times, various naturalists, such as Taylor (1913), have assumed
that the older the group the greater will be its range. Exceptions
occur to both these rules but they frequently afford valuable clues
in tracing the history of a group.

Species arise chiefly by an accumulation of gene mutations
(chromosome aberrations have not been investigated in
Amphibia). The genes are the hereditary factors and they lie in
linear order in the chromosomes. They have been compared with
catalysts and their size and number estimated in the case of the
fruit fly (Muller, 1929). Although naturalists have frequently
assumed that the hereditary material may be altered by the
environment, the proof of such an alteration is a matter of recent
demonstration. Muller and others have shown that X-rays
and radium may induce mutation in the fruit fly and other organ-

THE BIOLOGY OF THE AMPHIBIA

isms including plants. Goldschmidt (1929) has induced a
series of mutations in Drosophila by exposing the eggs for short
periods to a temperature of 37°C. Whether or not air tempera-
tures or radioactive substances in the earth have any influence on
mutation in Amphibia, it should be noted that the mutations so
far induced in animals or plants are no more adaptive to partic-
ular environmental conditions than the usual mutations of the
laboratory. Adaptation results from the fact that nature
permits those individuals to survive which are equipped with
useful or at least non-harmful mutations. Indifferent mutations
make up the bulk of specific differences. Darwin considered
specific differences to have been gradually improved by natural
selection, but more recent field observations have failed to show
the survival value of many characters, such as the color dif-
ferences of the various species of Ambystoma or Plethodon. The
red and gray phases of P. cinereus, for example, are nearly equally
abundant in regions where enemies, such as the screech owl, are
known to be abundant. It would thus appear that physiological
differences, such as habitat or breeding-season preferences, which
actually throw a derived stock out of competition with its ances-
tral form, are the real characters favored by natural selection.
Linked with the genes which determine these physiological
characters are still other genes which determine the visible
differences.

Natural Selection. — The great variety of apparently useless
characters found in Amphibia is due to the nature of the heredi-
tary mechanism. In other groups of animals it has been shown
that each gene may produce several visible effects. Some of
these may be favorable, others neutral, but they are either
accepted or rejected as a unit by nature. The survival of any
particular individual or species is not determined by the perfec-
tion of any one character but by the total fitness of an organism
for some particular environment. Since it is obvious that
natural selection weeds out those variants which are least fitted
to survive, we might expect that any species which has existed
in one environment for a long time would be as well-adapted as
its genetic constitution would permit. The possibilities of
viable mutations are, however, fewer than usually believed.
In spite of the fact that many groups of Amphibia were in
existence since the early Tertiary, we find many species still
bungling along with mechanisms not perfectly adjusted to any

SPECIATION AND ADAPTATION

one environment. The reason for this lack of complete adapta-
tion in all characters lies in the nature of the hereditary mech-
anism and the possibility for neutral characters being carried
along in the evolutionary stream.

It was noted by Darwin (1859) that wide-ranging species
usually exhibit more variation than forms having a smaller
range. These variations may show no intergradation with the
ancestral stock and in some cases have been given specific names.
Thus, Rana burnsi is a spotless Rana pipiens found in the same
locality as the latter and yet not intergrading (Weed, 1922).
In the same region Rana kandiyohi may be described as a mottled
Rana pipiens which does intergrade. In other groups of animals
mutations may show a perfect or incomplete dominance. In the
latter case the hybrids appear intermediate in character.

It is probable that both Rana burnsi and R. kandiyohi owe
their origin to one or more mutations but the determination
of the exact number will have to await a genetic analysis. The
adaptive value of the color differences, which is the distinguishing
character of these three species of Rana, is apparently very
slight; the same may be said of the color patterns of many other
species of Salientia. On the other hand, the coloration of
arboreal frogs and salamanders, which expose themselves to the
attacks of enemies, may be highly protective. Aneides aeneus,
for example, closely resembles the blue-green algae on the trees
it frequents, while Hyla andersoni has acquired the apple green
of the swamp magnolia on which it often rests. Such close
correlations owe their existence to natural selection and are
found in species most open to attack.

In the same way any rigorous habitat will foster more adapta-
tions than a less selective one. The tadpoles and salamanders
of mountain streams are equipped to hold tight and to expose
little surface to the current. They reduce their lungs which
might function as hydrostatic organs. The degree of adaptive
modification bears no relation to the degree of specialization
attained in their phylogeny. Ascaphus, America's most primi-
tive frog, lives in the mountain streams of northwestern United
States. In apparent adaptation to this habitat it has given up
its voice and reduced its auditory apparatus and lungs. The
males during the breeding season crawl along the bottom of the
streams in search of the females. External fertilization is
uncertain in swift currents, and the males of Ascaphus are

THE BIOLOGY OF THE AMPHIBIA

equipped with a vascular extension of the cloaca, which can be
carried forward and inserted into the cloaca of the female.
Although there are many mountain-brook urodeles, few Salientia
live habitually in these currents. One of the reasons may well
be that urodeles have adopted a method of internal fertilization.
Ascaphus has accomplished the same result by a different method.
Although Ascaphus is highly adapted to a mountain-brook
habitat, it retains all the primitive features of anatomy which
disclose its true relationships. The habitus characters of
Amphibia are not to be confused with the heritage of less plastic
features which indicate the phylogenetic position of the species.

Divergent Evolution. — A species is usually distinguished from
a subspecies by the arbitrary criterion that the former does not
intergrade while the latter always merges gradually into its
nearest relatives occupying contiguous ranges. Most species
are also distinguished from subspecies by the fact that they are
unable to cross with their nearest relatives. This sterility which
emerges with the birth of a species seems to be a consequence of
the difference in many genes; the greater the number of different
genes the more the likelihood of incompatibility on fertilization
or during development of the hybrid. Whenever two groups of
individuals are effectively isolated they tend to accumulate
different mutations, merely by chance, and hence continue to
diverge. Obviously, once this infertility is complete the oppor-
tunities for divergence are greatly increased.

Parallel Evolution. — One of the most interesting features of
speciation is that the same characters frequently appear inde-
pendently in the descendants of a single stock. This phe-
nomenon has frequently been noted in plants (Vavilov, 1922)
and in many groups of animals. It is even a feature of the
evolution of the opalinid parasites in the recta of frogs (Metcalf ,
1928). It is also an important characteristic of amphibian
speciation, as examination of the data in Chap. V will show.
For example, Boulenger (1918) in considering the subspecies of
the common European frog, Rana esculenta, showed that R. e.
chinensis repeated the principal characters of R. e. lessonae
although both are independently derived from R. e. ridibunda.
An even better case is found in the West Indian tree frogs.
Several species of Hyla in Hispaniola have been evolved inde-
pendently of the Jamaican series from a common Hyla brunnea-
H. dominicensis stock and in both islands certain distinctive

SPEC I AT I ON AND ADAPTATION

Fig. 28. — Parallel evolution. The life history data indicates that the large
tree frogs, Hyla lichenata (A) and H.vasta (C), have been independently evolved
from smaller ancestors, H.brunnea (B) and H .dominicensis (D), respectively.
Nevertheless, the larger species agree among themselves not only in size but in
their rhomboid pupil and rough skin. Many other instances of the independent
origin of identical characters may be found among the frogs and toads.

THE BIOLOGY OF THE AMPHIBIA

characters of pupil form, skin rugosity, and body size have
independently evolved in the derived species on these islands
(Fig. 28). In many groups of animals the reappearance of the
same character in species not closely related has given rise to the
suggestion that one species may be mimicking another which
has certain other characters of survival value. This mummery
has been brought about by the action of natural selection on
small mutations. In the Amphibia many characters of denti-
tion, pupil form, pectoral girdle, tongue form, digital scutes,
digital loss, etc., have reappeared in groups not closely related.

It would seem that the various
families of Amphibia had only
a limited repertoire of germ-
inal changes. Many of these
parallel changes have no
known functional significance.

In some cases the retention
of a character once it has re-
appeared in a different stock
may be aided by natural selec-
tion. Some polypedatid and
hylid tree frogs from different
parts of the world may appear
almost identical externally,
ntx ■ " . . . , , and it is possible that the

Fig. 29. — Mimicry in salamanders. 1
A reddish cheek patch is characteristic slow weeding Out of natural

of Plethodon jordani (B) and appears as
a variation in specimens of Desmognathus
fuscus carolinensis (A) living in the Great a b O U t

Smoky Mountains, the habitat of the however, would seem to have

former species. 7

had little effect on shaping
the color pattern of some Amphibia. For example, Plethodon
jordani of the Great Smoky Mountains is dark bluish with
a conspicuous reddish cheek. Desmognathus fuscus carolinen-
sis of the same region occasionally shows an almost identical color
pattern (Fig. 29). It would seem remarkable that this distinc-
tive color pattern should have occurred in two species in the
same region, but at Durbin, West Virginia, bright orange
specimens have been found, others with a stripe on each side and
a plain back, or a stripe on each side and a row of spots in the
middle of the back, or a series of small vermiculations on the side,
or several other distinctive patterns which are well-marked even

selection has brought this
Natural selection,

SPEC I AT I ON AND ADAPTATION

in young metamorphosed individuals. Some of these color
patterns appear again in species of Plethodon and Eurycea.
It is thus clear that D. f. carolinensis is able to produce in a single
locality many of the patterns of the Plethodontidae, and while
some of these patterns may appear with intergrades such as the
reddish-cheeked variant of the Great Smokies, others may show
little intergradation. If any of these well-marked color variants
of Durbin could isolate themselves in a distinctive range or
ecological niche, few systematists would hesitate in calling them
species.

The case of reddish-cheeked Plethodon and Desmognathus
occurring together in the Great Smokies and nowhere else in the
United States has been considered an instance of mimicry.
The phenomenon may be
compared with the parallel
modification of bent terminal
phalanges in certain African
ranids (Fig. 30). Why the
only species of Rana having
claw-shaped terminal phal-
anges actually perforating the
integument of the digit tips
should be found in the only FlG- f -Th° African Gampsosteo-

J nyx batesi with recurved terminal
part of the World where this phalanges which normally protrude
modification OCCUrS in Other through the skin of the toes to form

claws.

genera not closely related to

it is difficult to account for on the basis of natural selection,
since neither this modification nor the reddish cheeks seem to
have a survival value. It is possible that parallel modifica-
tions in unrelated genera are linked with physiological muta-
tions having such a value, but at present there is no evidence
for such an assumption.

Function in Phylogeny. — Structural characters may also
exhibit in some cases an apparent gradual change, in others an
apparent sudden modification. Various genera of frogs differ
from their closest relatives merely by a loss of teeth, but tooth
loss in some bufonids such as Batrachophrynus was brought on
gradually. Similarly, while the salamanders Manculus, Hemi-
dactylium, Salamandrella, and Salamandrina differ from their
ancestral stocks chiefly or at least in part by lacking the outer
toe of each hind foot (Fig. 31), toe reduction in Batrachoseps

THE BIOLOGY OF THE AMPHIBIA

pacificus and some species of Hynobius is a variable phenomenon.
Related frogs with and without the teeth apparently take the
same food. Similarly, no functional change has been noticed
in the locomotion of salamanders which have lost the outer digit.

Fig. 31. — Four-toed salamanders. The loss of the fifth or outer toe has
occurred frequently in the phylogeny of the salamanders. Four-toed species
of three different families are shown here: A. Hynobius keyserlingi. B. Hemi-
dactylium scutatum. C. Salamandrina terdigitata.

Tree frogs of Santo Domingo which have a rhomboidal pupil
and other species with an oval pupil are both nocturnal; and since
both live in the same valley, they would seem to have had little
reason for difference in the shape of the pupil. Whether a

SPECIATION AND ADAPTATION

character has taken its final form gradually or suddenly, natural
selection would frequently seem to have played little part in its
genesis. The effect of natural selection may, however, be
indirect, in the present instance favoring frogs of different sizes,
and the rhomboidal pupil may be another manifestation of the
gene or genes producing large size. Although the subject is
highly speculative, it is important to emphasize that many
characters of Amphibia have no functional significance but
nevertheless have appeared independently several times in
phylogeny.

Adaptation. — Most Amphibia are well adapted to the particular
environments in which they live. These adjustments have
been brought about by the elimination over a long period of time
of those variants which decreased the efficiency of the species
in any particular locality. Species are therefore preadapted by
gene mutations, very few of the great many mutations produced
(to judge from the kinds of variations in any one species) being
retained in future generations. As indicated in Chap. Ill,
function may play an important part during the later stages of
ontogeny in shaping certain organs or tissues of the body. There
is, however, no evidence that this effect is ever inherited. For
example, the blind salamander, Typhlotriton spelaeus as a larva,
lives chiefly near the mouths of caves and it retains functional
eyes throughout larval life. During metamorphosis, however,
it penetrates deeply into the caves and soon the lids draw
together, fuse in part, and the rods and cones of the retina
degenerate (Fig. 32). If the larvae are kept in the light during
this critical period they retain and further develop both the
functional eyes and pigmentation (Noble and Pope, 1928).
Typhlotriton has been losing its eyesight every generation for
presumably a very long period, since it represents one of the most
primitive plethodontids, and yet the effect of cave life has not
been inherited. Give the young, metamorphosed Typhlotriton
the stimulus of light, and it will develop functional eyes (Fig. 32).
The same is true to a lesser extent of the European blind sala-
mander. Proteus will redevelop cutaneous pigment in the light
(Werner, 1892) and further develop its larval eyes under certain
conditions of red and white light not to be expected in nature
(Kammerer, 1912). Although many modifications produced
during ontogeny resemble heritable features of other species,
this is no evidence that the modification frequently repeated

THE BIOLOGY OF THE AMPHIBIA

can impress itself on the germ. Thus, while cold has been shown
to induce the European land salamander to retain the young for
longer periods in the oviducts even until metamorphosis (Kam-
merer, 1907) and this condition is typical of the related Sola-
mandra atra (a high mountain species), Lantz (1927) found
that the former species, S. salamandra, may sometimes also
produce metamorphosed young in nature at a moderate elevation.

Fig. 32. — The influence of light on the eye of the cave salamander, Typhlo-
triton spelaeus. A. A blind adult reared in the dark for 203 days after the
beginning of metamorphosis. B. Another, reared in the light for approximately
the same period, retains and further develops the functional eyes both possessed
while larvae.

Mutations in other groups of animals have frequently been found
to resemble modifications, but there is no experimental evidence
that modifications produced during life in the body can be
transferred to the germ plasm and become hereditary. Those
who believe this possible would postulate long periods of time to
accomplish this result. The evidence available is, however,
against such an assumption (Cuenot, 1925).

Preadaptation. — Instances of preadaptation are given in the
discussion of behavior (Chap. XVI) and in the origin of the brood-
ing habit (Chap. XVII). The " sucking discs" of tree frogs are

SPECIATION AND ADAPTATION

frequently considered highly adaptive organs. They are really
adhesive and friction discs equipped with a series of glands and
a network of fine grooves (Chap. VI). Each cell is free distally
from its neighbor and being stiffened by a fibrous modification
of its cytoplasm catches in irregularities of the surface in much
the same way as the fine bristles covering the toe pads of gecko
lizards. Further, there is a series of fibers within the pad which
automatically squeeze the fluid from the glands when the body
weight of the frog pulls on the gripping toes (Noble and Jaeckle,
1928) . This modification of glands, epidermis, and pad fibers was
found to be present in frogs such as Phyllobates, which do not
climb, and others such as Acris, which have given up the arboreal
habits of their tree-frog ancestors. In general, tree frogs must
have pads of a certain size in order to be able to climb, but there
is little correlation between the actual width of the pad and the
amount of tree climbing the species practices. In general, large
frogs ascend to greater heights than small frogs. Hyla vasta
adheres with difficulty to the side of a glass aquarium, while the
much smaller H. crucifer may adhere for days, nevertheless the
former species lives in tall trees, while the latter rarely if ever
climbs at all. Possibly small frogs become desiccated more
quickly and hence are forced to keep near the ground. According
to Gadow (1901), the European tree frog lives the first two years
of its postlarval life in the grass. It would be interesting to
know if other tree frogs were terrestrial before they reached a
certain size in their ontogeny.

Salamanders which habitually climb trees have the digits
either more or less webbed or joined by a thick pad as in Oedipus,
or the terminal phalanges may be Y-shaped and bent downward
as in Aneides. Nevertheless, many other salamanders can readily
climb smooth vertical surfaces. The climbing salamanders are
few, and although one species of Aneides is apparently entirely
terrestrial (Storer, 1925) it is not clear that their climbing equip-
ment arose first in terrestrial species, as seems certain in the case
of the frogs. Many tree frogs have broad webs which may assist
in climbing, while others, chiefly the South American genus
Phyllomedusa, may reduce the webs and transform both hands
and feet into gripping organs. The latter would seem to be a
modification closely correlated with arboreal life. Webbed feet
are also found useful in the aquatic medium, and digital reduc-
tion, if on a different plan, occurs in many different families of

96 THE BIOLOGY OF THE AMPHIBIA

Salientia whose habits are apparently very distinct one from
another.

A B

Fig. 33. — Burrowing toads. Fossorial toads of several different families
resemble one another in their narrow, pointed heads and conspicuous 'spades,'
the digging tubercles of the hind feet. A. Hemisus marmoratum, a brevicipitid.
B. Rhinophrynus dorsalis, a bufonid.

The integument, which is the tissue first to come into contact
with the environment, might be expected to show the greatest

number of adaptations. But
Protopipa and Pipa from the
ponds of Guiana have a very
different degree of skin rug-
osity. Hyla vasta and Eleu-
therodactylus inoptatus live in
the tall trees of Hispaniola
and yet the first has a rough
and the second a smooth skin.
Smooth-skinned toads such
as Bufo alvarius of Arizona
live only near water, while
rough-skinned species may be
found far from water in the
desert. Thus, the structure
of the integument apparently
restricts the range of the spe-
cies, but the correlation be-
tween skin structure and
environment is not always
close. Many Salientia (Figs.
33 and 34) burrow to avoid
desiccation. The Spade-foot Toads are equipped with large
metatarsal tubercles which are doubtless of great assistance in this

Fig. 34. — Toad faces. The wedge-
shaped heads of burrowing toads are
variously modified. In Rhinophrynus
dorsalis (A) the snout is truncate; in
Rhombophryne testudo (B) it is covered
with sensory papillae.

SPEC I AT ION AND ADAPTATION

operation. Salientia of other families may be similarly equipped,
and some forms such as Helioporus and Chiroleptes make more
or less permanent underground passageways. The latter genus is
remarkable for its ability to absorb water rapidly until it assumes
the rotundity of a tennis ball (Buxton, 1923). The Australian
aborigines were found by the Horn Expedition to use these toads
as a source of drinking water.

Some burrowing species such as the Spade-foot Toads, Sca-
phiopus and Pelobates, have blunt, bony heads, the subcutaneous
tissues of the head being infiltrated with bone tissue. A similar
casque develops in species such as Hyla dominicensis, which only
rarely burrow. Other burrowing species have sharp, narrow
snouts with or without dermal ossifications. The aquatic
salamander, Amphiuma, is a notorious burrower and its sharp
snout and long body would seem to be produced expressly for
this purpose. Batrachoseps, which may be considered a long-
bodied Plethodon with a lost or reduced outer toe, is not, however,
more of a burrower than Plethodon glutinosus. Further, the
long-bodied Siren does not burrow at all. Still, Pseudobranchus,
a close relative of Siren, having a much more pointed head, readily
burrows into the sand covering the bottom of aquaria. The long-
bodied fish are looked upon as having evolved from short-bodied
forms under a variety of ecological conditions. Occasionally
the long body in both fish and salamander is put to some special
use, but neither seems to have evolved in correlation with the
burrowing habit alone.

Physiological Characters. — Many adaptations are not morpho-
logical but apparently physiological. Why should Salamandra
salamandra avoid limestone while Proteus and Typhlotriton
five well in limestone regions? Within the genus Eleuthero-
dactylus some species, as lentus, are found only in limestone
regions, and others never in such situations. The rough-skinned
Hyla arenicolor is found on rocks close to streams, while the
smaller and apparently more delicate Hyla regilla has a wide
range in many kinds of habitats (Storer, 1925). The factors
which hold Rana virgatipes and Hyla andersoni to the Atlantic
Coastal Plain are not known, but they would seem in some
way associated with the acidity of the water (Noble and Noble,
1923). Many cases of habitat preference, however, would
seem to evolve several factors. The Gopher Frog, Rana aesopus,
for example, breeds in the same ponds as several species of Rana,

THE BIOLOGY OF THE AMPHIBIA

but it alone leaves these ponds for a solitary life at the entrance
of Gopher Turtle burrows.

Although no determination has been made of any of these
factors, it was found that temperature may be of importance in
restricting the range of Typhlotriton to the vicinity of caves
(Noble and Pope, 1928). This species will not stand tempera-
tures so high as Eurycea multiplicata, which is found in the same
caves, and which, on the other hand, ranges far beyond the caves
in regions where water temperatures are considerably higher.
Presumably temperature limits the northern distribution of
many species of Amphibia and no forms are found in northern
regions where the subsoil remains permanently frozen throughout
the year.

As indicated in the discussion of the endocrine organs (Chap.
XIII), cold may prevent the functioning of the thyroid, and
various urodele larvae at high altitudes may become neotenous.
The adaptation of perennibranchs to the aquatic habitat is due
to the failure of the tissues to react to the thyroid hormone. This
condition has apparently been brought about by genetic factors.
It is, nevertheless, interesting to note that thoroughly aquatic
frogs such as the Bullfrog, Rana catesbeiana, and such tropical
species as Pseudis paradoxa usually have a longer larval life
than species which become terrestrial on metamorphosis. Simi-
larly, the aquatic Eurycea bislineata has a more extended larval
period than the more terrestrial Ambystomas. It would seem
that slowly maturing thyroid glands in the larvae are in some way
correlated with more or less aquatic preferences in the adult.

Hormones in Evolution. — It is not known whether genetic
factors have produced species of Amphibia by controlling the endo-
crine organs alone. Nevertheless, in many different genera, pairs
of species live side by side, one form half or less the size of the other
and approximating the young of the larger species in appearance.

In Cuba the diminutive Bufo dunni agrees well in form and
color with the young of B. peltacephalus of the same island. It
has not the cranial ossifications of the adult of the latter, but
these ossifications develop slowly during adult life in B. peltace-
phalus, and one would not expect to find them in a derived form
which had ceased to grow much beyond metamorphosis. Simi-
larly, the diminutive Necturus maculosus lewisi (Fig. 35) is a
dwarf derivative of N. m. maculosus living in an adjacent area.
In some cases the dwarfism is correlated with mountain life.

SPECIATION AND ADAPTATION

The dwarf species of Oedipus have large nostrils, not in adapta-
tion to any particular needs of mountain life but merely because
large nostrils characterize the young of Oedipus. These species
are essentially forms which have failed to grow up as do the
primitive species of the genus. This phenomenon of arrested
development has been recognized for a long time in various groups
of vertebrates (Franz, 1927). Cope (1889) made extensive
comparisons between the young and adult stages of various

Fig. 35. — Speciation by dwarfing. An adult Necturus maculosus lewisii (A)
compared with an adult N .m.maculosus (B) drawn to the same scale. The
former race has apparently developed from the latter by dwarfing.

genera of frogs. When species living in contiguous areas are
compared and the adults of one species found to agree closely
with the young of the other, it would seem probable that the
phenomenon of arrested development had played an important
part in the genesis of the smaller species.

Many characters of adult frogs resemble ontogenetic stages in
other species. Hyla vasta develops an extensive web between its
fingers (Fig. 36) and dilates its sacral diapophyses during post-
metamorphic life. Can the short webs and narrow sacral
diapophyses of some species of Hyla be considered arrested stages
of more primitive larger species? All specific changes appear
first during ontogeny. New species are not produced by the
addition of stages to more primitive species but by a modifica-
tion of the processes of development of the former. This
modification may mean a loss of growth, an extension of the

100

THE BIOLOGY OF THE AMPHIBIA

growth period, or a disharmonic growth of parts. Hence, if
two species are found together in the same or adjacent areas and
one never develops beyond a juvenile stage in the ontogeny
of the other, it does not always follow that the former species
has been derived from the latter. It is equally possible that the
reverse is the case and the " adult" characters represent a further
modification of the ontogeny characteristic of the other species.
It is also possible that the pair of species may have evolved
according to Eimer's principle of epistasy by which one of two

Fig. 36. — The growth of digital webbing in a tree frog after metamorphosis.
Left manus of Hyla vasta viewed dorsally : A . Adult. B. Recently metamorphosed
individual of the same species.

related forms becomes more modified in phylogeny than the other.
The bright salmon tints of the spring salamander, Pseudotriton,
may have been derived from the more primitive Gyrinophilus
danielsi. The purple salamander, G. porphyriticus, has similar
bright colors in some recently metamorphosed individuals,
however. Hence, the bright colors of both danielsi and Pseudo-
triton may be the retention of a juvenile character of G. porphyriti-
cus. In such cases a knowledge of the evolution of the group as
a whole and its routes of dispersal will sometimes afford important
evidence as to which possibility is more probable.

SPECIATION AND ADAPTATION

101

Phylogeny is the result of ontogeny; specific differences occur
in the genes of the eggs or sperms of the species, and they produce
effects which become more manifest as development proceeds.
Genes may occur which induce modifications only during larval
life. For example, although the species of Megalophrys appear
to be closely related, the larvae of some species differ remarkably
from the larvae of others. On the whole, however, evolution
has proceeded more rapidly in the adult than in the larval forms
and hence we have been able to conclude that the structure of
the larva may afford better evidence of relationship than many
adult characters (Chap. III).

Ontogeny does not repeat phylogeny. Amphibian larvae
in their external gills, adhesive organs, and body form resemble
the larvae of crossopterygian and dipnoan fish but not the adults.
This repetition of characters in corresponding stages is evidence
of relationship in the same way that the distinctive brevicipitid
larva common to Gastrophryne and Microhyla shows that these
genera are related. The brevicipitid larva has not the slightest
resemblance to an adult ranid from which the Brevicipitidae
evolved, and, as Garstang (1922), Sewertzoff (1927), and Franz
(1927) have recently emphasized, the adult stage of the ancestor
is not pressed back into earlier stages of development in the
descendants of any groups of animals. Over a century ago,
von Baer concluded that the young stages in the development
of an animal were not like the adult stages of other animals
lower down on the scale but were like their young stages, and
this conclusion seems equally well founded today.

Nevertheless, certain characters distinctive of an adult stage
may appear earlier in a descendant. This may be due to the
earlier functioning of the genes producing these characters, but
there are various conditions of development of Amphibia which
may also be considered. While the primitive frogs have arciferal
pectoral girdles, the more specialized frogs show firmisternal
girdles which are formed by two halves coming together to fuse
in the midline during ontogeny. This is apparantly the only
way possible for the firmisternal girdles to develop while main-
taining a lateral position in connection with the forelimbs. The
branchial arches of amphibian larvae bear a resemblance to
those of fish. Some frogs may skip the tadpole stage and in
these cases the arches may develop directly into the hyobran-
chials without serving as respiratory structures. There is a

102

THE BIOLOGY OF THE AMPHIBIA

recapitulation of successive grades of differentiation but the
repetition of ancestral adult stages is usually lacking during
ontogeny. Nevertheless, bone may replace cartilage during
development, or the anlage of originally separate organs may
form separately and fuse later. As Garstang (1922) has pointed
out, it is this formative dependence of one organ or tissue on
another which confers upon ontogeny its recapitulative character.

Permanent Larvae. — Growth and differentiation, as discussed
in Chap. XIII, are controlled by the hormones of the glands of
internal secretion. The relation of hormones to the genes is
well shown in the phenomenon of metamorphosis. At this
period the salamander larva and the frog tadpole undergo an
extensive reorganization and differentiation and emerge as
tetrapods capable of land life. The gills are lost, the branchial
clefts fused, the larval branchial skeleton is changed into the
adult hyobranchial. The eyes bulge, lids are formed, palate,
jaws, and skull bones undergo marked changes. In the tadpole
the larval epidermal teeth are lost, the tail is absorbed, while in
urodeles the spike teeth of the larva are usually replaced by
bicuspid ones, and the fin on body and tail is reduced. Wilder
(1925) has described some of the many changes which take
place at the time of metamorphosis in the larval Eurycea bislineata.
Not all of these occur in other species. For example, the maxil-
lary bones are formed long before metamorphosis in the axolotl
but not in Eurycea. Endocrinologists seize upon the shedding
of the skin in one or more large pieces as the criterion of meta-
morphosis in the urodeles. Correlated with this skin change the
large Leydig cells are lost and the stratum corneum develops as
an adaptation to resist the drying effect of the air.

Some urodeles never metamorphose and others seem to begin
the process and not complete it. When incomplete metamorpho-
sis occurs, it is not due to the absence of the thyroid hormone,
which induces metamorphosis in other species, but to the fact
that certain tissues are no longer sensitized to this hormone.
These tissues do not react to thyroid extracts injected into the
animals' bodies (Chap. XIII). For the present discussion it is
interesting that the hyoid apparatus of Necturus and Amphiuma
on its first appearance has the reduced form of the adult of these
species just as if not enough branchial arch-forming material
had been present (Noble, 1929). Further, the palatoquadrate
bar in Siren splits into the usual two parts at a time when the

SPECIATION AND ADAPTATION

103

skin retains its typical larval structure. Although the physio-
logical block to complete metamorphosis in these permanent
larvae is not known, it is obvious that structural changes are
taking place at such early and disconnected stages that they
cannot be considered metamorphosis. Nevertheless, if we focus
our attention only upon the most obvious changes of meta-
morphosis, namely the development of limbs, of maxillary bones,
the loss of gills, and reduction of branchial arches, Siren and
Pseudobranchus would be considered forms which have ceased to
differentiate beyond a very early stage of larval life; Proteus
and Necturus, forms which have reached a later stage of urodele
ontogeny; Cryptobranchus, one which has begun its metamorpho-
sis; and Megalobatrachus and Amphiuma, forms which have
nearly completed their metamorphosis. If we examine the skin
of the last three genera it will be found to have metamorphosed
completely and thus run ahead of this scheme. Further, the
skin of the adult Siren has the typical metamorphosed structure
while that of the closely related Pseudobranchus is larval. The
skin of Necturus does not react to the thyroid hormone, while
that of Cryptobranchus does (Noble and Farris, 1929). There is,
of course, little advantage to be gained by the latter change since
both of these genera are entirely aquatic. The thyroid hormone
reacts on tissues which are sensitized to its action, and this
sensitization is produced presumably by genetic factors without
any relation to the future use of this modification.

The thyroid hormone may produce its influence on metamor-
phosis very indirectly. For example, Maurer (1921) found that
removing the forelegs of a tadpole did not prevent perforations
from developing in the operculum during metamorphosis. He
assumed that this could be explained only on the basis of the
inheritance of acquired characters, the forelegs having been
pushed presumably through the operculum for so many genera-
tions that now the holes would form even when no legs were
present. But Helff (1924) showed that the perforation of the
operculum was due to a secretion of the degenerating gills which
would induce a similar histolysis of the integument on other parts
of the body. Thus, the thyroid hormone by inducing a degenera-
tion of the gills caused the production of a cytolysin which released
the forelimbs. An even more complex situation is to be found in
the tail of a tadpole during metamorphosis. If skin from the
body region is transplanted to the tail before metamorphosis,

104

THE BIOLOGY OF THE AMPHIBIA

this piece of skin does not degenerate with the remainder of the
caudal appendage at the time of transformation (Reis, 1924).
In addition to the hormones producing metamorphosis, there
are cytolysins released which are specific for certain skin, namely
that of the tail, but have no effect on other skin which differs
structurally in no essential way. Since moreover, skin from the
anterior part of the tail grafted to the back of frog tadpoles under-
goes histolysis at a greater speed than skin from near the tail
tip similarly grafted, there exists a gradient of response to these
cytolysins in the skin of the tail (Clausen, 1930). The tail is
not absorbed from the tip forward as commonly supposed; the
degeneration of tissue is more rapid at the base. Metamorphosis
even within the tail of Amphibia is a very complex process.

The Course of Phylogeny. — It may be noted by referring to
other sections (Chap. I, Part II) that neoteny in the usual sense
of the word, namely the retention of larval characters during
sexual maturity, has played no part in the phylogeny of the
Amphibia. Typhlomolge is a plethodontid salamander because
it possesses characters in common with plethodontid larvae.
Necturus and Proteus are isolated in a separate family of Caudata
by taxonomists because they possess several striking features
not shared by other salamanders, larval or adult. These perenni-
branchs owe their position in the system to the degree they have
diverged from apparent ancestors and not because of their
larval features per se. The more advanced types of any group
of animals are frequently highly modified and consequently
restricted to particular environments but it does not follow that
primitive types are always more "plastic," more able to cope with
varying conditions of habitat. Ascaphus, the most primitive
frog in America, can live only in or near cold mountain streams.
Primitiveness rests on resemblance to ancestral types and not at
all on any physiological peculiarities.

In tracing the evolution of the Amphibia (Chap. I) we noted
various trends of evolution, especially the reduction in the number
of skeletal elements and the increase in cartilage. The latter may
be described as a progressive foetalization. Similarly, the loss
of teeth in various groups of Salientia may be considered a reten-
tion of a larval condition, since teeth in other Salientia do not
appear till metamorphosis. The same process of progressive loss
may be traced in the evolution of higher classes of vertebrates.
Another parallel is to be found in the secondary production of

SPECIATION AND ADAPTATION

105

snakelike forms. In salamanders and lizards, the elongation
of the body in phylogeny is accompanied by the reduction in the
length of the limbs. Among the Amphibia these elongate types
have not proved highly efficient, at least they have not split
up into many species, while in the Reptilia the success of the
snakes is familiar to everyone. Similarly, the birds which are
specialized reptiles have succeeded extraordinarily well and
show the danger of concluding that a specialized group is in any
way senescent.

References

Boulenger, G. A., 1918: On the races and variation of the edible frog,
Rana esculenta L., Ann. Mag. Nat. Hist. (9), II, 241-257.

Buxton, P. A., 1923: " Animal Life in Deserts; A Study of the Fauna in Rela-
tion to the Environment," London.

Chapman, Frank M., 1926: The distribution of bird-life in Ecuador, Bull.
Amer. Mus. Nat. Hist., LV, 784.

Clausen, H. J., 1930: Rate of histolysis of anuran skin and muscle during
metamorphosis, Biol. Bull., LIX, 199-210.

Cope, E. D., 1889: The Batrachia of North America, Bull. U. S. Nat.
Mus., No. 34.

Cuenot, L., 1921: "La genese des especes animales," 2d ed., Paris.

, 1925: "L'adaptation," Paris.

Darwin, Charles, 1859: "Origin of Species," New York.
Fisher, R. A., 1930: "The Genetical Theory of Natural Selection," Oxford.
Franz, V., 1927: Ontogenie und Phylogenie, Abh. theor. Organ. Entw., Ill,
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Garstang, W., 1922: The theory of recapitulation: A critical restatement

of the biogenetic law, Jour. Linn. Soc. London, XXXV, 81-103.
Goldschmidt, R., 1929: Experimentelle Mutation und das Problem der

sogennannten Parallelinduktion. Versuche an Drosophila, Biol.

Zentralbl., XLIX, 437-448.
Grinnel, Joseph, 1924: Geography and Evolution, "Ecology," V, 225-229.
Haecker, V., 1908: Uber Axolotlkreuzungen; II, Mitteilung (Zur Kenntnis

des partiellen Albinismus), Verh. deutsch. zool. Ges. 18. Vers., 194-205.
Helff, O. M., 1924: Factors involved in the formation of the opercular leg

perforation in anuran larvae during metamorphosis, Anat. Rec, XXIX,

102.

Jordan, D. S., 1926: Isolation with segregation as a factor in organic evolu-
tion, Ann. Rep. Smithson. Inst., 1925, 321-326.

Kammerer, Paul, 1912: Experimente iiber Fortpflanzung, Farbe, Augen
und Korperreduktion bei Proteus anguinus Laur, A rch. Entw. Mech.,
XXXIII, 349-461, 4 pis.

Kellicott, W. E., 1907: Correlation and variation in internal and external
characters in the common toad (Bufo lentiginosus americanus), Jour.
Exp. Zool, IV, 575-614.

Lantz, L. A., 1927: Quelques observations nouvelles sur l'herpetologie des
Pyrenees centrales, Rev. Hist. Nat. Appl, VIII, 16-22, 54-61.

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THE BIOLOGY OF THE AMPHIBIA

Matthew, W. D., 1915: Climate and evolution, Ann. N. Y. Acad. Sci.,

XXIV, 171-318.

Maurer, F., 1921: Zur Frage von der Vererbung erworbener Eigenschaften,

Anat. Am., LIV, 201-205.
Mertens, Robert, 1926: tiber Farbungsmutationen bei Amphibien und

Reptilien, Zool. Am., LXVIII, 323-335.
Metcalf, M. M., 1928: Trends in evolution: a discussion of data bearing

upon "orthogenesis," Jour. Morph. Physiol., XLV, 1-46.
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Muller, H. J., 1929. The gene as the basis of life, Proc. Int. Congr. Plant

Sci., I, 897-921.

Noble, G. K., 1929: Further observations on the life-history of the newt,

Triturus viridescens, Amer. Mus. Novit., No. 348.
Noble, G. K., and E. J. Farris, 1929: A metamorphic change produced in

Cryptobranchus by thyroid solutions, Anat. Rec, XLII, 59.
Noble, G. K., and M. E. Jaeckle, 1928: The digital pads of the tree frogs;

A study of the phylogenesis of an adaptive structure, Jour. Morph.

and Physiol, XLV, No. 1, 259-292.
-Noble, G. K., and R. C. Noble, 1923: The Anderson tree frog (Hyla ander-

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II, 417-455.

Noble, G. K., and S. H. Pope, 1928: The effect of light on the eyes, pig-
mentation and behavior of the cave salamander, Typhlotriton, Anat.

Rec, XLI, No. 1, 21.
Okada, Y., 1928: Notes on the breeding habits of Rhacophorus in Japan,

Annot. Zool. Japon., II, 279-285, 1 pi.
Piersol, W. H., 1929: Pathological polyspermy in eggs of Amby stoma

jeffersonianum (Green), Trans. Roy. Canadian Inst., XVII, 57-74, 1 pi.
Reis, K., 1924: Sur le comportement des greffes de la peau dans la queue du

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Rensch. B., 1929: "Das Prinzip geographischer Rassenkreise und das

Problem der Artbildung," Berlin.
Robson, G. C., 1928: The species problem: An introduction to the study of

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Manuals, No. VIII, Edinburgh.
Sewertzoff, A. N., 1927: tiber die Beziehungen zwischen der Ontogenese

und der Phylogenese der Tiere, Jena. Zeitschr. LXIII, 51-180.
Shelford, V. E., 1913: The reactions of certain animals to gradients of

evaporating power of air: A study in experimental ecology, Biol. Bidl.,

XXV, 79-120.

Storer, T. I., 1925: A synopsis of the Amphibia of California, Univ. Cal.

Pub. Zool, XXVII, 1-343, 18 pis.
Taylor, J. W., 1913: Geographical distribution and dominance in relation

to evolution and phylogeny, Trans. Congr. Ent. Oxford, II, 271-294,

pis. 6-9.

Vavilov, N. L., 1922: The law of homologous series in variation, Jour.
Gen., XII, 47-89.

SPECIATION AND ADAPTATION

107

Weed, Alfred C, 1922: New frogs from Minnesota, Proc. Biol. Soc.
Wash. XXXV, 107-110.

Werner, Franz, 1892: Untersuchungen liber die Zeichnung der Wirbel-
thiere, Zool. Jahrb. Syst., VI, 155-229, 5 pis.

Wilder, I. W., 1925: "The Morphology of Amphibian Metamorphosis,"
Smith College, Northampton, Mass.

Witschi, E., 1930: Studies on sex differentiation and sex determination in
Amphibians; IV, The geographical distribution of the sex races of the
European grass frog (Rana temporaria L.); A contribution to the
problem of the evolution of sex, Jour. Exp. Zool., LVI, 149-166.

CHAPTER V

SEX AND SECONDARY SEX CHARACTERS

Sex is the physical, chemical, and psychical difference between
male and female animals. The difference is primarily correlated
with the production of male and female sex products and the
facilitation of their union. Sexual reproduction hastens evolu-
tion, for it combines the characters existing in a population in a
variety of different ways and brings new mutations into relation
with old combinations, thus giving natural selection more
kinds of individuals on which to work. It is thus biologically
important that the egg should not develop until it receives the
male chromosomes in the process of fertilization. As discussed
in Chap. II, frogs' eggs may be made to develop in other ways, but
under natural conditions the egg does not divide until activated
by a spermatozoon.

The sexual characters form a well-defined group, usually
sharply distinguished from somatic characters both in structure
and function. The genetic analysis of these characters in animals
other than Amphibia has shown conclusively that they owe their
origin to changes in the same chromosomal mechanism which
through its mutations has produced the somatic characters
(Crew, 1927; Morgan, 1926). Various other explanations have
been given for the origin of secondary sexual characters in Amphi-
bia, but none of these fits the facts of sexual divergence as
exhibited by related species. These divergences may be con-
sidered in some detail, for they have an important bearing on the
origin of characters in relation to the use which is finally made
of them.

Under the term " secondary sexual characters" are included all
the differences between the two sexes other than those connected
with the gonads and their ducts. The latter are considered in
the chapter dealing with the urogenital system. The best-known
secondary sexual characters are the nuptial pads which appear
on the prepollex region of many frogs and toads during the breed-
ing season, or the bright colors and crests of certain male European

108

SEX AND SECONDARY SEX CHARACTERS 109

newts during the same period. These, like the majority of second-
ary sexual characters of vertebrates, are brought to expression by
the hormone of the testes (Chap. XIII). Many, such as the
elongate, premaxillary teeth of Desmognathus, are potentially
present in both sexes and can be made to develop in an adult
female if a testis is transplanted into the body. The hormone
acts upon characters determined by heredity but able to develop
only in the presence of the testicular hormone. Other secondary
sexual characters resemble those of invertebrates in that they
do not require the testicular hormone to maintain their appear-
ance. It is interesting that this should be true of certain characters,
such as the vocal pouch of Rana esculenta (Champy, 1924) which
has a great functional value in the male, and also equally true
of others, such as the cloacal papillae of certain newts (Naka-
mura, 1927) which have a doubtful functional significance.
Both those characters dependent on a testicular hormone and
those independent of it find their hereditary determiners in
genes and hence may be considered together in the present
discussion.

Functional Significance of Secondary Sex Characters. — It is

well known that the nuptial pads of frogs are used for main-
taining a firm grip on the back of the female during egg laying.
Pads are also present on the upper arm of the male Pleurodeles
which swims below his partner during the courtship (Chap. XVI).
This would seem to be an inappropriate position to take but it is
actually well adapted to the method of fertilization by spermato-
phores. The male, after a time, frees one foreleg and by bending
his body forward deposits a spermatophore opposite the female's
snout. The male P. waltl then crawls forward until the female's
cloaca is directly over the spermatophore. In P. poireti there is
a circling movement with the clutched arm as the pivot leading
to the same result (Klingelhoffer, 1930). It is interesting that
the male Salamandra grips the female the same way, although
courtship proceeds on land (Van Leeuwen, 1907). The hedonic
glands, found on the tails and other parts of the body of male
plethodontids (page 136) and on the cheeks of the male Triturus
viridescens, are other mechanisms nicely adjusted to play a certain
part in the complex courtship of these animals. The method of
courtship varies with each group of salamanders, and hence differ-
ent secondary sexual characters might be expected in the various
groups.

110

THE BIOLOGY OF THE AMPHIBIA

Instinctive habits, often quite different in the two sexes,
appear during the breeding season under the influence of gonads
and may be classified as secondary sexual characters. In the
Salientia, associated with the greater activity, louder voice,
and retentive grip of the male sex, many structural differences
of fluctuating or more permanent character may appear. The
forelimb bones may be greatly molded by the muscles of the
male as in Leptodactylus ocellatus (Fig. 37) and Rana spinosa, and
less pronounced skeletal differences have been found between

Fig. 37. — Sexual dimorphism of the forelimbs in the South American frog,
Leptodactylus ocellatus. A. Female. B. Male.

the sexes of almost all Salientia which have been intensively
studied (Dauvart, 1924; Kandler, 1924; Klier, 1926; Harms,
1926; Sailer, 1927). There are correlated differences of muscle
weight (Gaule, 1900). The abdominal muscles of the male
have such an important function in forcing air from the lungs
in producing the call and are correspondingly more powerful
than those of the female, but differences are also to be found
even in the tendons of the two sexes (Kahn, 1919). The lungs
of many male frogs are larger than those of the female, markedly
so in Bombina (Boulenger, 1897). This may be correlated not
only with the louder voice but also with the higher metabolism
and greater activity of the male. The red blood count of the
male frog is higher (Zepp, 1923), its brain weight greater (Komine,
1924), its liver heavier (Yunge, 1907). In the case of the
African Astylosternus robustus, a species with greatly reduced
lungs, a compensatory vascularization of the integument occurs
in both sexes, while in the male patches of vascular villosities
appear on the thighs and sides, and in reference to these the species
has been given the name of " Hairy Frog" (Fig. 63). These
villosities apparently supply the frog with the greater amount of

SEX AND SECONDARY SEX CHARACTERS 111

oxygen his sex demands (Noble, 1925). The difference between
the sexes of frogs may thus extend to many details of their anat-
omy and physiology and may include many little-understood
differences, such as the shorter intestines of the male of some
European frogs (Yunge, 1907). Sex differences may be demon-
strated in the functioning of the heart (Appelrot, 1930) and these
may possibly find their explanation in the higher calcium content
of the tissues of the male frog. A similar variety of secondary
sexual differences may be found without doubt in urodeles.
Ueki (1930) noted that the sexual differences occurred in many
parts of the viscera, brain, and eyes of the Japanese newt,
Triturus pyrrhogaster. Although these modifications probably
have some functional correlation, it is difficult to account for
the much softer skin of the male, since neither secretions nor
rubbing movements are known to play a part in the courtship
of this species.

As indicated in the discussion of habits (page 410), the methods
of courtship and embrace are singularly uniform through-
out the Salientia, differences appearing only in the position of the
forelimbs about the body or the relation of the fists to the female's
body or to each other. Nevertheless, the differences in the
nuptial pads of closely related species may be extraordinary.
The nuptial pads usually consist of a cluster of black epidermal
spines covering a swelling on the prepollex region of each hand.
The swelling is formed by numerous acinous glands having a dis-
tinctive granular cytoplasm at the height of the breeding season.
Some species, such as Bufo vulgaris, lack the glands (Kandler,
1924), and others, as Hyla arborea and Hemisus marmoratum,
may lack the asperities. Pigmented breeding pads have extended
to the mesial surfaces of the three inner digits in some species of
ranids and bufonids. Spines similar in appearance to those
on the pad may rarely occur on various parts of the appendages,
as along the edges of the toe webbing in Discoglossus, or along
the toes in Pelodytes, or as patches on three of the toes in
Bombina variegata. They also occur under the toes in a position
where they could not function in certain higher forms such as in
Hyla leprieuri (Boulenger, 1912). Pigmented spines occur on
the ventral surfaces of the forelimbs in the breeding males of
some discoglossids, pipids, and ranids. They extend to the
chest and chin of a few discoglossids, pelobatids, bufonids, and
ranids. In the case of certain species of Rana this spread of the

112

THE BIOLOGY OF THE AMPHIBIA

spiny area to the chest is correlated with a life in mountain
torrents. In such situations the ability to maintain the grip
on the female is placed at a premium, and Pope (1931) has shown
that the frogs breeding along certain Chinese torrents either had
spiny chests or the males were much smaller than the females
and hence offered little resistance to the current when carried
on their backs. The tendency to form pigmented spines in the
male is by no means always correlated with obvious advantages.
In fact, the tendency seems to run riot in the males of some frogs,
for the spines may appear on almost any part of the body. The
males of one or more species of Bufo, Hylambates, Chiromantis,
Megalixalus, Phrynobatrachus, and Eleutherodactylus have their
dorsal surfaces covered with spines, while the females are smooth
above. In many of these species no asperities at all appear on
the prepollex and hence the dorsal rugosity cannot be considered
an extension of the nuptial pad area. If sex recognition in these
species is accomplished by trial embrace, as in Rana sylvatica
(Noble and Farris, 1929), the dorsal spines might serve the
courting male to distinguish quickly between the sexes. Such
an explanation does not work out well in detail, for while the
male, Bufo marinus and B. regularis are more spinous above, the
females of Bufo funereus, B. vulgaris, and B. americanus are
the more spinous or rugose. In Bufo canorus the male has both
fewer and smaller warts than the female (Storer, 1925). In
other genera also the differences between the skin of the two
sexes may be great or slight according to the species, making it
doubtful if skin "feel" could play a part in sex recognition
throughout the group.

In various salamanders there may be a difference of texture
in the skin of the two sexes. The western " water dog, " Triturus
torosus, as well as the above-mentioned T. pyrrhogaster, is much
smoother skinned in the male. Fisher (1905) showed that " dur-
ing the fall the dermis of the female frog is thinner and less resist-
ant to acids and alkalis and digestive fluids than that of the
male." Zepp (1923) found that the skin of certain European
frogs (excluding that of the head) was much heavier in the male
sex. Such differences might be assumed to be correlated with
the chain of anatomical differences alluded to above and to have
no specific functions in the breeding act.

Unexplained Sexual Differences. — Such an assumption would
not explain the spinosity of other species of frogs. For example,

SEX AND SECONDARY SEX CHARACTERS 113

the males of some African tree frogs, as Megalixalus fornasinii
and M. leptosomus, are spinose above, while spines of similar
character are found over the dorsal surfaces of both sexes of
the closely related Megalixalus spinosus. Although these spines
are slightly better developed in the breeding male, they are an
important feature in both sexes and represent an instance of a
phenomenon frequently found in birds and mammals where a
character found only in the males of one species appears fully
developed in both sexes of another (Pycraft, 1914).

A similar phenomenon is to be observed in the European newts.
In various species (italicus, montandonii, etc.), the males have
the tip of their tails extended into a whip lash which may serve
to direct the secretion of the abdominal glands toward the female
during courtship, although other species seem to get along with-
out the lash. This secondary sexual character appears in both
sexes of the related T. palmatus where its function in the female
is a mystery. Other cutaneous hypertrophies in Amphibia
present equal difficulties when their possible functions are
considered. For example, the male European toads, B. vulgaris
and B. viridis, exhibit a slight extension of the webbing between
the toes during the breeding season. This involves a growth of
the toe and tarsal ridges to form fringes in the male Pelodytes
punctatus, while in the male Elosia and Crossodactylus a similar
hypertrophy produces broad folds. In the wood and grass frogs
of America and Europe, (Rana sylvatica, temporaria, etc.), the
toe webbing of the male is extended to form a convex edge during
the breeding season, but a detailed study of the breeding of the
first species did not give proof of the use of these structures
(Noble and Farris, 1929). If we assume that all of these toe
webs must be used in some way in swimming, we have still to
account for their sporadic occurrence in only one or two species
of very distinct families. Any explanation in terms of function
is complicated by the fact that a slight seam appears along the
fingers of both the male Crossodactylus and Elosia in the breed-
ing season. Further, in Crossodactylus gaudichaudii the second
finger of the male is spatulated, while in Phyllobates nubicola
(Dunn, 1924) it is the third finger which is thus modified. If
field observations should demonstrate that these broadened
fingers are pressed against the female in amplexus, we have still
to explain why female frogs from the other side of the world
have a similar modification. For in Lechriodus melanopyga

114

THE BIOLOGY OF THE AMPHIBIA

(Fig. 38) the two inner fingers are spatulated, while in Limno-
dynastes dorsalis the second finger is broadly spatulated and the
third hypertrophied along its preaxial edge.

Although certain modifications of the appendages would
seem to have considerable use, they are frequently found in

Fig. 38. — Secondary sexual modification of the manus in Lechriodus melano-
pyga. A. Right hand of female as seen from below. B. Right hand of male,
same aspect.

only a few species of a related group. The European mountain
brook newts of the genus Euproctus are notorious in the way
they court. The males lie in wait among the rocks and snare
passing females with their prehensile tails. So forceful and pro-

Fig. 39. — The male Triturus pyrrhogaster with the glandular hypertrophies, the
elongated digits, and the pointed tail, characteristic of this sex.

longed is the grip that it frequently kills the captured animal.
E. montanus apparently assists the grip with the spikelike
processes which protrude from its fibulas (Klingelhoffer, 1930).
Nevertheless the related E. asper succeeds well without these
spurs. Again, the toes of some newts, especially those of Triturus

SEX AND SECONDARY SEX CHARACTERS 115

vittatus and T. pyrrhogaster (Fig. 39), are elongated in the breed-
ing males. These apparently balance themselves on their digit
tips while waiting expectantly for a female. The attitude is,
however, not very different from the usual posture of aquatic
salamanders when on the alert. It is difficult to believe that
male salamanders "well up on their toes" have a decided advan-
tage in courtship or that the elongated digits per se have a great
selective value.

Perhaps the most discussed secondary sexual characters of
vertebrates are the color differences. Darwin tried to explain
these differences in birds by his well-known theory of sexual
selection, the female being supposed to select the most attractive
male and hand on his characters to her male progeny. Such a
selection has been denied in fishes (Kyle, 1926) although in some
groups sexual differences in color seem to aid sex recognition*
In the European newts, which have bright colors in the male,
there is a certain amount of display which apparently tends
to raise the female to such a state of sexual excitement that she
will pick up the spermatophore when it is later emitted by the
male. But in the blind salamander of Europe, Proteus anguinus,
two rows of light spots appear on the side of the tail during the
breeding season (Chauvin, 1883) and these certainly would not
be appreciated by his sightless mate. In all Salientia where the
courtship and mating has been adequately analyzed, sight has
been found to play almost no part in sex recognition (Noble and
Farris, 1929) other than to inform the male of the approach of
another object of suitable size or movement. Nevertheless,
some species as distantly related as Bufo canorus of the Yosemite
(Storer, 1925) and Arthroleptella lightfooti of South Africa (Rose,
1929) may show a marked difference in color and color pattern
in the two sexes. Some differences of color may be directly
correlated with physiological changes which take place in the
male during the breeding season. Thus Leydig (1892) showed
that in both Rana fusca and Triturus cristatus the dermis of
the integument undergoes a marked swelling in the breeding
male. This is not due merely to an absorption of water, for
while the lymph spaces increase in size the lymph becomes
gelatinous in some of the spaces. The yellow color of the throat
of the male Cricket Frog, Acris, and the dark tone of breeding
toads' throats are correlated with the enormous expansibility
of this region during the breeding season. Still, such seasonal

116

THE BIOLOGY OF THE AMPHIBIA

changes would not account for the marked sexual difference in
color pattern seen in some frogs and salamanders.

Most Amphibia, unlike lizards and birds, show little or no
sexual difference in color. Male lizards make great use of their
conspicuous colors in bluffing possible rivals, while many birds
engage in elaborate courtship displays. In most vertebrates

Fig. 40. — Secondary sexual characters in Old World frogs. A. Left manus of
Dimorphognathus africanus as seen from below, showing the elongated third
finger of the male. B. Head of the male of the same species with the pseudo-
teeth of the lower jaw characterizing this sex. C. Head of the male Petropedetes
newtonii showing the columella process, the spike-like metacarpal I and distinc-
tive chin spines. D. Head of Rana pileata with the frontal swelling peculiar to
the male.

where marked sexual differences in color appear these have an
important role in sex recognition or courtship. The types of
courtship found in Amphibia are usually not such as would foster
a sexual divergence in color.

Phylogeny of Secondary Sex Characters. — The phylogeny of
other secondary sexual characters is instructive when considered

SEX AND SECONDARY SEX CHARACTERS 117

in relation to the apparent phylogenies of the various species.
Although the more familiar frogs and toads have the prepollex
region of the male covered with a nuptial pad, the prepollex itself
or the adjacent digits may be modified into a spine or " dagger"
in other species. In Petropedetes newtoni the metacarpus of the
first digit is enlarged, spikelike, and protrudes through the skin

Fig. 41. — Closely related frogs frequently have markedly different secondary
sexual characters. The forelimb of the male Hoplophryne uluguruensis (A)
compared with the forelimb of H. rogersi (B), seen from the same ventral aspect.

as an effective instrument for holding the female (Fig. 40C).
In Telmatobius jelskii the same element is enlarged, in Dis-
coglossus it is broadened, while in Leptodactylus ocellatus it is
bifid with two spines. In other frogs it is the prepollex which is
hypertrophied to form a recurved spine. There is no 'evidence
of a progressive enlargement of this spine in any Salientia. For
example, in the recently described " Banana Frogs" of East
Africa, a pad of sharp dermal spines occurs on each side of the
chest in the male Hoplophryne uluguruensis and another cluster
of large dermal spines over the prepollex region of each hand
(Fig. 41 A). Such a formidable array of spines rarely occurs in

118

THE BIOLOGY OF THE AMPHIBIA

any frog, and one would imagine that this diminutive frog was
amply equipped to hold his own with any struggling female.
But in the closely related Hoplophryne rogersi of an adjacent
mountain range, the rudimentary prepollex of uluguruensis
has enlarged to form a formidable spine (Fig. 4 IB).

An equally convincing case of the discontinuous nature of
prepollex region modifications in frogs is seen in the hylids of
Santo Domingo. There is considerable evidence to show that
these species represent a closely related group which evolved from
a single stock. Nevertheless, the prepollex region is differently
modified in each species. Three species have dermal
spines, and in Hyla heilprini alone a formidable prepollex
" dagger" appears. Equally interesting is the fact that the
prepollex of the not closely related Hyla maxima and its allies
of South America is hypertrophied into a similar recurved dagger
in the male, as well as in Hyla pollicaris of the Bismark
Archipelago. Further, a similar enlarged prepollex appears in
the male of the brevicipitid Phrynella pollicaris and the ranid
Rana holstii. Since species with and without the daggers are
not known to hold their hands in a different manner, the case seems
exactly comparable to the change in pupil form in the same hylas
of Santo Domingo. As pointed out in the previous chapter,
one species has developed a radically different shape of pupil and
a similar modification has independently evolved in a different
stock of tree frogs.

Many other cases of parallel evolution, or, better, the appear-
ance of the same modification in not closely related species, may
be found among the secondary sexual characters. For example,
a sharp, recurved spine appears on the proximal end of the
humerus in Hyla humeralis but in none of the closely related
species of the same region, while an identical spine reappears in
the male Centrolene on the other side of the world but is not
found in any of its relatives living in that region. All plethodon-
tid salamanders possess hedonic glands which serve to attract
the females (Chap. XVI). These glands usually manifest
themselves as a swelling on the chin, or as a scattering of enlarged
glands on the lower eyelid, or along the cheeks of the male. In
Eurycea multiplicata they form a prominence on the dorsal surface
of the tail base which appears even in the male larva (Fig. 42C).
An apparently homologous glandular appendage develops above
the base of the tail in Salamarpdra caucasica and S. luschani,

SEX AND SECONDARY SEX CHARACTERS 119

members of a different although ancestral family. Turning to
the Salientia, many cases of glandular hypertrophies are found
in the male sex but none is known to play any part in attracting
the female. All species of Cycloramphus (Fig. 42B) have gland-
ular pads in the inguinal region, and similar but more extensive
glands appear on the sides of the body of Hyla rosenbergi. Pelo-
bates has a pad of glandular tissue on the outer side of the upper
arm where it could not function in the embrace, and a similar
pad crops up in many species of Rana (the Hylorana group).
In the African tree frogs, Leptopelis rufus and L, aubryi, sl pair of

Fig. 42. — Hypertrophied glands as secondary sex characters. The glandular
mass at the tail base of the male Eurycea multiplicata (C) is employed to attract
the female. The functional significance of the hypertrophied glands on the
thighs of the male M antidactylus luteolus (A), viewed ventrally, and in the inguinal
region of the male Cycloramphus asper (B) is at present unknown.

glandular patches appears on the chest of the male and would
be assumed to function in holding the female. But in various
pelobatids (Scaphiopus, Cophophryne, and some Megalophrys), a
similar pair of pads appears in both sexes. Perhaps this is another
instance of the inheritance of male characters by the female, but
the Pelobatidae are far more primitive than the polypedatid
tree frogs and hence presumably represent the primitive condi-

120

THE BIOLOGY OF THE AMPHIBIA

tion. In this connection we might compare the inguinal glands
of Cycloramphus with those of Pseudophryne guentheri. In the
latter they appear in both sexes, but most developed in the large
females. In Bufo punctatus the paratoid glands, which would seem
to. have no direct role in the breeding process, are most pronounced
in the male. Whatever may be the function of these various
glandular hypertrophies it is interesting that they crop up in
unrelated families, sometimes in both sexes and again only in one.

The males of many species of the neotropical frog, Leptodacty-
lus, develop a pointed snout with a horizontal ridge along the
upper lip during the breeding season. This strange modification
of the head into a veritable spade is apparently correlated with
the practice of digging holes near the edge of streams or ponds
in which the females, attracted by the calls of the male, may come
and lay their eggs. It is interesting from the phylogenetic
standpoint that a very similar modification of the snout reappears
in Batrachylodes vertebralis, a frog of a very different family
living on the other side of the world (Mertens, 1929). This is
another instance of similar secondary sexual modifications
reappearing in unrelated groups. It is exactly comparable to
the occurrence of balloon-like external vocal pouches on each
side of the lower jaw in diverse species of Leptodactylus, Hyla,
and Rana.

Have these secondary sexual characters come into existence
by a slow progressive change and do they represent only the final
stages of specialization left on the earth today? This may be
true in some but not in all cases. For example, the European
toads, Bombina bombina and B. variegata, are very closely related
and yet only the former possesses vocal pouches (Mertens, 1928).
Again one of the most bizarre secondary sexual characters is
found in the African Petropedetes newtoni. Here the columella is
thrust through the drum of the male and, covered by the derm,
it forms a prominent projection (Fig. 40C). There are five
species in the genus but only newtoni exhibits this peculiar struc-
ture. P. newtoni agrees with many other Salientia in that it has
apparently suddenly developed a very distinctive type of second-
ary sexual character. The modification is further surprising in
that the eardrum shows very little sexual dimorphism throughout
the Salientia. In the Bullfrog, Rana catesbeiana, the Pond Frog,
Rana clamitans, and allied species, the eardrum of the male is
distinctly larger than that of the female (Fig. 43). This is a

SEX AND SECONDARY SEX CHARACTERS 121

case where a secondary sexual character is found throughout an
allied group of species and stands in striking contrast to the
conditions in Petropedetes. Why the male frog would have need
of a more elaborate hearing organ than the female is not at all
clear.

Fig. 43. — Sexual dimorphism in the Bullfrog, Rana catesbeiana. The tym-
panum is markedly larger in the male (A) than in the female (B) of the Bullfrog
and allied species.

Relation of Secondary Sexual to Somatic Characters. — The

secondary sexual characters of Amphibia are highly discontinuous
in their occurrence. Further, almost identical modifications
may appear in unrelated groups. The only adequate theory
which will explain the origin of secondary sexual characters
is that they are due to gene mutations which occur either in the
sex chromosome or in the autosomes but in the latter case can
come to expression only in the male or the female body, as the
case may be. Natural selection has tended to preserve those
mutations which facilitate sexual union, but just as in the case
of the somatic changes some mutations have given rise to
"neutral" characters, those which are neither harmful nor useful,
but which are carried along by the hereditary stream. There
are several possible ways by which a sex-linked or sex-limited
character may lose this bondage to one sex and appear in both.
Genetic evidence as to the nature of this change is lacking for the
Amphibia. Nevertheless, the fact that this change has occurred
not once but many times in Amphibia as well as in other verte-
brates throws considerable light on the origin of certain somatic
characters.

This point of view may be made clearer by further illustration.
In the evolution of the Dusky Salamanders, Desmognathus, from
the large D. quadra-maculatus to the small D. fuscus ochrophaeus

122

THE BIOLOGY OF THE AMPHIBIA

and D. fuscus carolinensis, the male exhibits an increasing ten-
dency to lose its vomerine teeth in adult life and to reduce the
anterior part of the parasphenoid tooth patches. Leurognathus
marmorata intermedia, which has been derived from D. quadra-

Fig. 44. — The reappearance of male characters in both sexes of other species.
The nuptial spines, usually characteristic of the male frog, occur in the female
Crossodactylus gaudichaudii {A) nearly as well developed as in the male (B).
The vomerine teeth are lacking in the male Desmognathus fuscus (D) but present
in the female (E). In the related Leurognathus marmorata marmorata (C) both
sexes lack vomerine teeth. The skulls are viewed ventrally, the forelimbs
dorsally. Pt., parasphenoid teeth patches; Vt., vomerine teeth.

maculatus, has the vomerine teeth absent in the males like the
more advanced species of Desmognathus. In L. m. marmorata
this loss occurs in both sexes and is called a " specific character"
(Fig. 44). The loss might be considered an adaptation to aquatic
life except that the terrestrial D. /. carolinensis and the aquatic
L. m. intermedia both show the initial stage in tooth loss. Again,

SEX AND SECONDARY SEX CHARACTERS

123

it has recently been shown that the males of some and possibly
all species of Eurycea hypertrophy the teeth in both jaws from
short bicuspid teeth, characteristic of most metamorphosed
Amphibia, to elongate monocuspid ones (Fig. 45). It had

Pr.Fr. Sph. Fr.

Fig. 45. — Secondary sex differences in the skull, especially in the teeth, of the
two-lined salamander Eurycea bislineata bislineata. A. Female. B. Male.
Devi,., dentary; Fr., frontal; Mx., maxillary; Na., nasal; Op., operculum; Par.,
parietal; Per., periotic; Pmx., premaxillary ; Pr.Art., prearticular; Pr.Fr., pre-
frontal; Pt., pterygoid vestige; Qu., quadrate; Sept., septomaxilla; Sph., sphe-
nethmoid; Sq. squamosal.

previously been pointed out that the males of most plethodontids
have the premaxillary teeth elongate, monocuspid, and directed
more or less forward (Fig. 46). A possible use for the latter
modification was found in courtship of Eurycea bislineata (Noble,
1929) where during the initial stage the male rubs the female

124

THE BIOLOGY OF THE AMPHIBIA

with his snout. No males, however, opened their mouths during
any phase of the courtship and no biting was observed even in
cases where courting pairs were crowded together in a small
aquarium. Hence the elongate maxillary and dentary teeth of
Eurycea seemed to have no specific function. In the related
Gyrinophilus no sexual differences in dentition appear. In
G. porphyriticus, the purple salamander, the teeth are all bicuspid.
In the closely related G. danielsi, however, the teeth of both jaws
are elongate and monocuspid. There is no evidence that these
two species of Gyrinophilus differ essentially in feeding habits,
and yet there is nearly as much difference in their dentition as
between the two sexes of Eurycea. If the elongation of the

teeth in the latter is merely
due to " neutral" genes which
happen to be sex-linked or
sex-limited, the occurrence of
a similar modification in both
sexes of G. danielsi would

Fig. 46. — The male Manculus quad- , ,

ridigitatus has the naso-labial grooves Seem to be due 10 Similar

of each side extended into a cirrus. As genes which, however, have
in many other plethodontids, the pre- -a A +u- T l A

maxillary teeth are elongated, directed avoided tniS linkage. An

forward, and exposed during the breed- apparent difference is never-
theless to be found in the
genesis of the teeth, since those of the male Eurycea fluctuate
with the season and are apparently under the control of the
sex hormone, while those of Gyrinophilus are not known to be
influenced by hormones.

The modification of the teeth of vertebrates is generally
believed to be closely correlated with changes in food habits.
Nevertheless, the most extreme types of dental modification in
Amphibia fail to show this correlation. Many cases of dental
change in the evolution of the frogs resemble those of urodeles.
For example, in the ranid Dimorphognathus africanus (Fig. 40B)
the premaxillary and maxillary teeth in the female are of moder-
ate length and bicuspid; those of the male are long and mono-
cuspid as in Eurycea. True teeth are lacking in the lower jaw
of Dimorphognathus as in all other ranid frogs, but this species
has hypertrophied the margins of the prearticular bone into a
series of pseudoteeth (Noble, 1922; Fig. 3). The similarity of
this sexual modification of teeth with that of Eurycea extends
even to a certain seasonal fluctuation in the form of the teeth in

SEX AND SECONDARY SEX CHARACTERS 125

the upper jaw. No male frogs are known to fight with their
teeth for the possession of the female, nor do rubbing movements
of the jaws as in Hydromantes (Fig. 47) play any part in court-
ship so far as is known. Hence, as in the case of Eurycea, a func-
tional significance for the dental hypertrophy is doubtful.
Nevertheless, the same apparent changes in linkage seen in the
plethodontids occur in frogs. In the neotropical Hemiphractus
and Amphodus, the dorsal margin of the prearticular is hyper-
trophied into a row of pseudoteeth in both sexes. Hemiphractus

Fig. 47. — The elongated teeth in the upper jaw of the male Hydromantes
platycephalus apparently serve as stimulating organs during courtship. The
males of other species of the genus rub the females with their chin and teeth during
this period.

goes farther than Dimorphognathus in the development of excess
bony growths, for its whole skull has become evolved in a gro-
tesque casque of secondary dermal bone.

The exact form of the tooth varies with the species in both
frogs and urodeles, although tooth characters have been rarely
used in defining species. The hypertrophy of the teeth is not
always correlated first with one sex and later with both. In
Ceratophrys the smaller species have bicuspid teeth in both
sexes; the larger, monocuspid elongate ones. In young speci-
mens of the large species such as C. dorsata, the teeth arise as
monocuspid structures. A similar loss of one cusp, apparently
the outer, occurs in the phylogeny of Aneides; the smaller species,
aeneus, having bicuspid teeth in both jaws for a long period, the
larger, lugubris, developing many monocuspid teeth directly.
On the other hand, many large species of both frogs and sala-
manders have bicuspid teeth, and small species, such as Leptopelis
brevirostris and Phrynopsis usumbarae as well as various pipids,
have elongate monocuspid ones, showing that there is no correla-

126

THE BIOLOGY OF THE AMPHIBIA

tion between body size and tooth form throughout the Salientia.

Although dental modifications may or may not be sex-linked,
the question arises: Do structures well known to be functional
in the male ever appear in the female of another species where
they cannot possibly have these functions? The best-known
peculiarity of the male frog is the cluster of asperities which
appear on his thumb during the breeding season. These organs
serve to maintain the grip of the male on a struggling female and
consequently would have no use in the latter sex. Nevertheless,
in Crossodactylus gaudichaudii conspicuous black spines appear
on the thumb of the female and while they are usually not quite
so large as those on the male they are frequently more numerous
(Fig. 44 A). Similarly, a large frog from Okinawa Island was
taxonomically isolated from the related species of Rana by
creating for it the name "Babina" merely because the female
frequently has its dagger-like prepollex as well developed as in the
breeding male. These cases of the appearance of male characters
in the female are directly comparable to the development of
horns in the female caribou. Characters which are sex-linked
or sex-limited in one group need not be so in another.

Discontinuous Evolution. — One of the striking features of the
secondary sexual characters of Amphibia is the way apparently
useful modifications are given up once they have been acquired.
For example, the male Desmognathus phoca has not only larger
maxillary teeth than the female but the lingual cusp is directed
posteriorly. Such a modification would apparently assist the
male in holding his grip on struggling prey. In the more advanced
D.fuscus carolinensis, however, the maxillary teeth are broadened
and the elongate cusp has been given up. Further, in a local
race of D. f. carolinensis which has been given the subspecific
name of imitator, the maxillary teeth of the male may revert to
the form of D. phoca. The Plethodontidae exhibit other instances
of the same " shuffling of characters." The primitive Eurycea
has monocuspid premaxillary teeth as previously described. In
the terrestrial Plethodon, a more advanced type, the males of
the larger species fail to show this modification. In the small
P. cinereus which was apparently derived from one of the larger
species (Dunn, 1926) the character has reappeared again although
on a different plan, for while the tooth is elongated, the outer
cusp is longer than the inner. Batrachoseps and Hemidactylium,
which were apparently both derived from Plethodon, have

PRIVATE LIBRARY OF
ALBERT G. SMITH

SEX AND SECONDARY SEX CHARACTERS 127

redeveloped the character in its typical form. Some western
species of Plethodon have the teeth monocuspid but directed only
slightly forward. If we assume that the larger species of Pletho-
don represent the primitive condition for the genus, both Batra-
choseps and Hemidactylium may be described as having
redeveloped a secondary sexual character found in Eurycea.

Many of the secondary sexual characters of Amphibia, espe-
cially modifications of the tooth form, skin texture, body propor-
tions, frontal enlargements, appendage form and length, body
coloration, and habits find close analogies in the sexual modifica-
tion of fish. Further, many fish and reptiles show the change of a
character from a sex-linked or limited one to a character of both
sexes. Familiar examples may be found in the horns of Chame-
leons which in some species occur only in the male; in others, in
both sexes, although the utility in either sex is very doubtful
(Hilzheimer, 1913). Some mammals have horns in one sex and
others in both and again the value of these structures in the
struggle for existence has been doubted by competent mammalo-
gists. The theories of Cunningham (1908) and Champy (1924)
fail when one attempts to trace the phylogeny of secondary sexual
characters; further, the experimental evidence lends little support
to their views (Morgan, 1919). Secondary sexual characters
apparently owe their origin to gene mutations; those characters
which happen to be useful in the breeding process are retained
by natural selection. As in the case of many specific characters,
a parallel change may occur in a not closely related group;
further, many characters seem to have no function but when
not harmful have been retained in association with more useful
mutations. Since the same character may appear in one sex
of one species and in both sexes of another, the utility of such a
character in courtship or mating becomes doubtful. On the
other hand, such a change in linkage presents further evidence
that many specific characters have arisen without relation to
definite functions. Since Darwin's time, characters have been
scrutinized with regard to their survival value. Where natural-
ists have failed to find such values, they have assumed that the
data were merely incomplete. Genetical studies have shown
that a single mutation of a gene may affect various parts of an
animal's body, producing changes in certain organs which render
these more efficient while they render others less important in
survival. The genes, moreover, are transmitted together in

128

THE BIOLOGY OF THE AMPHIBIA

groups. Hence, any mutation of great survival value might be
transmitted with a number of genes which produce distinctive
modifications but neutral ones in the struggle for existence. It
is important to consider these neutral characters, for upon a
change of environment or habit they may become highly adap-
tive. Amphibia in both their secondary sexual and somatic
characters are preadapted by gene mutations to new conditions
of living many of which conditions are never realized by any
particular species.

References

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cardio-inhibitory mechanism of frogs and toads, Amer. Jour. Phys.,
XCV, 242-249.

Boulenger, G. A., 1897: "The Tailless Batrachians of Europe,'' Part I,
London Ray Soc.

, 1912: On some tree-frogs allied to Hyla caerulea with remarks on

noteworthy sexual characters in the family Hylidae, Zool. Jahrb. Suppl,
15, I, 211-218.

Champy, Ch., 1924: "Les caracteres sexuels considered comme phenomenes
de developpement et dans leurs rapports avec l'hormone sexuelle," Paris.

Chauvin, Marie von, 1883: Die Art der Fortpflanzung des Proteus angui-
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Crew, F. A. E., 1927: "The Genetics of Sexuality in Animals," Cambridge
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Cunningham, J. T., 1908: The heredity of secondary sexual characters in
relation to hormones, a theory of the heredity of somatogenic charac-
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Dauvart, A., 1924: Ein bis jetzt unbekanntes zyklisches Geschlechts-
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Dunn, E. R., 1924: Some Panamanian frogs, Occ. Papers Mus. Zool., Univ.
Mich., No. 151.

, 1926: "The Salamanders of the Family Plethodontidae," Smith

College, Northampton, Mass.
Fisher, A. 0., 1905: Marked differences between the skin of the male and

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Gaule, J., 1900: Uber die geschlechtliche Differenz der Muskeln bei

Froschen, Arch. ges. Physiol, LXXXIII, 83-88.
Harms, Jiirgen W., 1926: "Korper und Keimzellen," Berlin.
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seine anatomische Grundlage und seine biologische Bedeutung, Zool.

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Kandler, Rudolf, 1924: Die sexuelle Ausgestaltung der Vorderextremitat
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Klier, A., 1926: Die Art- und Geschlechtsunterschiede am Becken und

Ober- und Unterarmknochen bei Rana temporaria und Rana esculenta,

Zeitschr. Anal. Entw., LXXX, 669-703.
Klingelhoffer, W., 1930: "Terrarienkunde," Lief. 13 and 14, Stuttgart.
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seasonal changes in the relative weight and the sex difference of the

central nervous system of Rana nigromaculata, Sci. Rep. Tohoku Imp.

Univ. Sendai., Japan Biol. Ser. I, No. I, 51-74.
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Salamandra maculosa Laur, Zool. Anz., XXXI, 649-653.
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Morgan, T. H., 1919: The genetic and operative evidence relating to

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CHAPTER VI

THE INTEGUMENT

Amphibians are provided with a soft, moist skin which, except
for that of the caecilians, is devoid of scales. The fish ancestors
of the Amphibia possessed scales and these were retained in
many of the first tetrapods. Some microsaurs possessed scales
over most of their body, and the caecilians seem to have inherited
this condition directly from them. Within the caecilian group a
reduction of the scalation has occurred, some genera retaining
scales only on the back and others lacking them entirely. The
scales of caecilians are small, averaging about 1.5 mm. in diameter.
They are hidden under the skin and not visible but, when revealed
by a needle, are found to resemble in form and sculpture one of
the types of scales found among the labyrinthodonts. In some
fish, scales are formed late in development, while in branchio-
saurs and caecilians they do not appear until the time of
metamorphosis.

A few extinct types, notably the labyrinthodont Dissorophus,
had bony plates along the back. A secondary deposit of bone
occurs in the skin of the head or back in various modern Salientia,
especially in burrowing pelobatids, buf onids, and hylids. As most
frogs use their hind legs and not their head in burrowing, it has
been claimed that the bony casque may act as a plug to the
burrow. A similar bony deposit has been found in species which
are not known to burrow, however, and no satisfactory explana-
tion has been given of either the origin or the function of these
bony deposits. The modification reaches its extreme in the
diminutive Brachycephalus, where the dorsal plate fuses with
the underlying neural spines, and in the grotesque Triprion, where
the bony growth distorts the face in an extraordinary manner.

The integument is far more than a wrapping around the body;
it is an organ of many functions. During early embryonic fife
the integument is represented merely by the ectoderm. Cilia
develop on its outer surface and these serve to pass a current
of fluid continuously over the embryo. The direction of beat is

130

THE INTEGUMENT

131

determined very early and is continued even when the ectoderm
is isolated from the underlying tissues (Twitty, 1928).

Unicellular Glands. — Shortly before hatching, a series of uni-
cellular glands appear on the snout of tadpoles and probably all
urodele larvae. They may extend along the back of some frog
embryos (Saguchi, 1915). In Xenopus (Bles, 1906), Alytes

Fig. 48. — The hatching of Alytes, the midwife toad. As in the case of other
Salientia, the tadpole escapes from the egg by digesting its way out. A. Section
of the frontal organ or digesting glands just before hatching. B-E., Several
stages in the hatching process; H.G.C., hatching gland cell; S.C., supporting cell.

(Noble, 1926), the axolotl (Wintrebert, 1928), and Ambystoma
opacum (Noble and Brady, 1930), it has been shown that these
glands function in producing a secretion which digests the egg
capsule and frees the embryos. It is due to the early develop-
ment of these unicellular glands (Fig. 48) that some frog tadpoles
hatch in a very immature condition.

132

THE BIOLOGY OF THE AMPHIBIA

Before the larva hatches, more or less of the ectoderm has
developed two layers of cells and is now designated as epidermis.
At the same time it has become closely attached below to a
membranous corium, or dermis, of mesodermic origin. The
epidermis of urodeles develops a series of large, glandlike cells
(the Ley dig cells), which seem homologous with the clavate cells
of fishes and which may serve to ward off infection (Wilder,
1925), although they are rarely seen discharging their secretion
(Dawson, 1920). In caecilians they frequently discharge on the
surface (Sarasin, 1887). The tadpoles of Salientia lack these
Leydig cells entirely.

Comparison with Fish. — The chief evolutionary advance
shown by the integument of the Amphibia over that of the fish
is the development of alveolar and, in some cases, of tubular
glands. There are two types of alveolar glands common to the
three orders of Amphibia. The first comprises the mucous
glands, which secrete a transparent substance to serve as a
lubricant in the water and to keep the skin moist on land. Mucous
glands are widely spread over the body and never reach a large
size, although under slight stimulation they produce a copious
flow. In some species, as the Slimy Salamander, P. glutinosus,
the secretion may be sticky. The second category embraces the
granular glands, which produce an acrid secretion, very injurious
to mucous membranes of the eye and mouth. The granular
glands usually require considerable stimulation to produce their
thick, milky secretion. They are often of large size and clustered
in pads such as in the paratoid glands of the common toad, or in
ridges, as along the back of many species of Rana. In terrestrial
salamanders they may form warts, as in Tylototriton, or merely
thickened portions of the integument of back and tail, as in
Plethodon.

It has been claimed that mucous and granular glands are
merely different growth stages of one type of gland. B/ut
Proteus develops only mucous glands, and various tadpones
such as those of Ascaphus may develop granular glands alone.
Further, there are marked differences in the histological structure
of the two glands (Dawson, 1920), the secretion of the mucous
glands staining with basic dyes, and never assuming the form of
granules, while the secretion of the granular glands stains readily
with plasma dyes and has a granular appearance (Fig. 49).
Both glands develop from the epidermis and in many species

THE INTEGUMENT

133

do not appear until shortly before metamorphosis. The
granular glands become surrounded by a muscular sheath
of epidermal origin, while the mucous glands in various species
remain without this cover. Both lie, for the most part, in the
corium which during development increases in thickness and
differentiates into three layers, the inner and outer layer being
more compact than the middle one. Besides glands, connective
tissue, and blood vessels, there is considerable smooth muscle in
the corium.

Fig. 49. — Vertical section of the skin from the dorsal surface of the tail base of
Plethodon cinereus showing three types of skin glands. Cap., capillary; D.,
dermis; Dt., duct of exhausted granular or poison gland; E., epidermis; H.Gl.,
hedonic gland (cut to one side of main axis); M.Gl., mucous gland; P., melano-
phore; P.Gl., poison gland; R.Gl., developing poison gland.

Poison Glands.— The granular glands of Amphibia protect
their owner from being devoured by many possible enemies.
The western newt, although terrestrial for a large part of the year,
is rarely eaten by either birds or mammals (Storer, 1925). The
poisonous properties of the glands have been studied critically,
especially in European and South American Salientia (Phisalix,
1922), but these properties do not always protect many toads
and salamanders from being eaten by snakes or even by
other Amphibia. Secretion from both the mucous and the
granular glands of many species is poisonous. Phisalix (1918)
found that the mucus of Hydromantesitalicus when injected into a
frog was more poisonous than the secretion of the granular glands.
Nevertheless, the chief function of the mucous glands is to keep

134

THE BIOLOGY OF THE AMPHIBIA

the skin moist, while that of the granular type is to protect the
possessor against being devoured. Toads, or other Amphibia,
cannot give warts and usually their secretions have no effect on
the unprotected hand. The West Indian Hyla vasta and the
African Phrynomerus bifasciata have been found under certain
circumstances temporarily to inflame the hands of the collector.
Both of these species produce great quantities of milky secretion.

Mucous glands of Amphibia function on the least excitation,
while the milky secretion of the granular glands requires pressure
or injury. The secretion of the mucous glands is usually color-
less in Amphibia, but it may be mauve rose as in Discoglossus
or brown as in the Mexican axolotl. The blue secretion recently
reported in a West Indian Eleutherodactylus (Dunn, 1926)
apparently came from mucous glands. The toxic substance of
mucous glands seems independent of the amount of mucin
released. The mucous secretions of Proteus and Siren are
innocuous, while that of many newts and frogs has an irritating
effect on eyes or nostrils when brought near them and a very
disastrous result when injected into the digestive tract of animals
(Phisalix, 1922; Biedermann, 1930).

The granular glands produce a secretion which is usually much
more toxic than that of the mucous glands. In the toad this
secretion may contain more than one poisonous constituent.
Faust isolated bufotalin, giving it an empirical formula of
C34H46O10. Bufotalin appears to be an oxidation product of
bufonin, a weaker poison, which apparently conditions the milky
appearance of the gland secretion. Abel and Macht (1912)
described bufogin, assigning to it the formula C18H24O4. Both
bufotalin and bufogin resemble digitalis in increasing the tonicity
of the heart, eventually leading to its stoppage. Administration
of the secretion of the granular glands of toads to the stomachs of
higher vertebrates causes nausea, a weakening of respiration, and
muscular paralysis. The secretion brought in contact with the
eye produces a serious inflammation.

The poisonous secretions of salamanders have also been
analyzed chemically. Three alkaloids have been extracted from
the granular glands of Salamandra. Samandarin, with the
formula C26H40N2O, affects the respiratory centers in the central
nervous system of dogs, but it is apparently not so abundant in
S. salamandra as another weaker alkaloid which has been given
the name "samandaridin." The poison from the granular

THE INTEGUMENT 135

glands of Salamandra air a differs from that of S. salamandra and
is called "samandatrin." These alkaloids have the same effect
as the natural poison.

Toad skins are used as medicine by the Chinese, and
their therapeutic value may not be wholly psychological.
Abel and Macht discovered adrenalin in the paratoid glands
of the toad. Apparently adrenalin was not secreted as such
by the gland, but resulted from a chemical change within
the mature secretion (Shipley and Wislocki; 1915). It is, never-
theless, remarkable to find adrenalin in an external secretion.

Species differ enormously
in the virulence of their
poison. It has been noted
(Wright, 1914) that the
common Pickerel Frog, R.
palustris, will frequently^kill
other species of fro^Samed
home in the sam^ar^rn it.
Many of th^, Vic^^rightly
colored ^$peci^ especially
those^^arJJ&& with yellow
and red, ^iave been found to
be highly poisonous, but
bright colors are not always
linked with virulent secre-
tions. Brazil and Vellard
(1926) found that the dull-
colored Ceratophrys americana
has a virulent poison, while
the gaudy C. dorsata has innocuous skin secretions. The
large Leptodactylus pentadactylus has bright thighs, but it
lacks the highly poisonous secretions of the drab-colored Bufo
marinus. The latter species produces one of the most virulent
poisons known among the Amphibia, one that frequently kills
dogs which have not learned to leave the toad alone. Whether
or not because of this poison, the Marine Toad is almost ubiqui-
tous in the American tropics.

Some species of the neotropical brachycephalid toad, Dendro-
bates, are bright green or pink, spotted with a dark tone. Their
secretions are used by Indians of Colombia as a source of poison
for their arrows. Whether these species are more poisonous than

Fr. Ep.

Fig. 50. — Diagram of a longi-
tudinal section of the toe of a tree
frog, showing the tree-climbing
mechanism. Fr.Ep., friction surface
of pad with its wedge-shaped super-
ficial cells; I.C., intercalary cartilage;
P.GL, friction pad gland.

136 THE BIOLOGY OF THE AMPHIBIA

other less conspicuous forms of the same genus is unknown.
Gadow (1901) points out that toads of this genus are used to rub
on the growing feathers of parrots to change them from green to
yellow.

Other Glands. — The mucous glands have apparently given
rise to a number of hypertrophied and often tubular glands of
special functions. Of these, the best known are the glands on
the thumbs or chests of various male Salientia during the breeding
season. Their secretion is more granular than that of ordinary
mucous glands and helps the male to maintain by adhesion his

grip on the female. The toes
of tree frogs are equipped with
pads which are not suction devices, as
frequently stated, but elaborate fric-
tion and adhesion mechanisms (Fig.
50). The superficial cells of the
epidermis are more or less free
one from the other and project
as so many short bristles against
the substratum. The pad is sup-
plied with a complex series of
tubular glands which pour their
adhesive secretion on the surface
of the pad.

Mucous glands have apparently
given rise during phylogeny to another
type of gland of totally different
functions. The male Plethodontidae
develop glands having a slightly
granular secretion which apparently
serves to attract the female. A
patch of these glands on the chin usually becomes enlarged
to form a conspicuous pad (Fig. 51).

The Plethodontidae are characterized by a naso-labial groove
which serves to free the nostril from water (Wilder, 1906). This
groove is flushed by a battery of tubular and frequently branched
glands which seem to represent merely a ventral extension of the
glandular area surrounding the nostril orifice of the species
(Fig. 52). The latter cluster of glands keeps the nostrils of
Amphibia free from water and dirt.

Fig. 51. — The glandular
area on the chin, the hyper-
trophied naso-labial glands,
and the elongated premaxillary
teeth are characteristic of the
males of several plethodontid
salamanders including Oedipus
adspersa, viewed here from the
ventral surface.

THE INTEGUMENT

137

Odors. — Many frogs and salamanders have distinctive odors.
The Mink Frog, Rana septentrionalis, receives its local name
from its odor. The Marsupial Frog, Gastrotheca monticola, has a
peculiar pungent smell, also reminiscent of that of a mink. It is
noteworthy that while the two pelobatids Pelodytes and Pelo-
bates, have the odor of onions (Boulenger 1911), the obviously
unrelated Salamandra salamandra and Bufo vulgaris are both
reported to smell like vanilla. The vanilla odor in Hydromantes

Fig. 52. — The naso-labial glands of plethodontid salamanders. The naso-
labial groove is a glandular furrow which serves to free the nostrils from water in
the plethodontid salamanders. The head of the Purple Salamander, Gyrinophilus
porphyriticus (B) , shows both naso-labial groove and lateral line organs. On the
left the skin (A) of the head of Desmognathus fuscus has been removed together
with the naso-labial glands and is viewed from the under surface. C.J., conjunc-
tiva; L., labial glands; L.L.O., lateral-line organ; N.L., naso-labial glands; N.L.Gr.,
naso-labial groove; N.L.M., cut end of tubule which lies in the groove of the
maxillary bone; N.L.P., tubule of naso-labial gland within the premaxillary
foramen. (A, after Whipple.)

italicus is produced by the granular glands (Phisalix, 1918).
The odor of Hydromantes genei is a sweetish, penetrating odor
which arises from these salamanders even when they are not
handled. All odors appear to arise from either the secretions
of the granular or mucous glands. Odors have not been reported
from tadpoles or salamander larvae, and in most of these the
glands do not become functional until shortly before metamor-
phosis. The mature tadpoles of Rana heckscheri, however, have
a peculiar sweetish odor. On the other hand, it is highly prob-
able that odors undetectable by our olfactory mechanisms are
present in Amphibia and play an important role in the economy
of some species. The secretions of the hedonic glands of newts
and plethodontid salamanders have no recognizable odor and yet
they seem to function in holding the attention of the female during
courtship. At the height of the courtship, one species of pletho-
dontid will not court with another, and since the male has been

138 THE BIOLOGY OF THE AMPHIBIA

observed to nose the female before rejecting her, specific qualities
of the skin secretions of the female are apparently recogniz-
able by the male (Noble and Brady, 1930). No distinctive
glands are present in the integument of the female and hence it
is, apparently, the odor of the ordinary skin glands which must
be acceptable to male plethodontids before they will begin the
courtship.

Horny Growths. — The epidermis during larval life is protected
by a cuticular margin on the outer layer of cells. At metamor-
phosis the epidermis usually increases in thickness and the outer
layer of cells flattens and cornifies. It is interesting that some
fish, such as Periophthalmus, which have adopted terrestrial
habits should have developed a protective cover of horn (Harms,

Fig. 53. — The larva of Onychodactylus japonicus, showing modification of the
limbs for mountain-brook life. The tips of the digits are equipped with recurved
claws and the broad fin occurs on the post-axial margin of the limbs.

1929). The metamorphosis of the epidermis in Amphibia is
not induced by drying as one might expect (Wilder, 1925), but is
regulated by the thyroid hormone. Siren and Cryptobranchus,
which are considered larval types, have succeeded in metamor-
phosing their integument but not all of their other structures.
They thus remain aquatic forms although equipped with a thick-
ened epidermis, having the superficial layer cornified.

A cornification of limited portions of the epidermis occurs in
various larvae in a highly adaptive manner. The digit tips of
various mountain-brook species of hynobiids, ambystomids, and
plethodontids are covered with thickened and partly horny
epidermal caps. In Onychodactylus larvae (Fig. 53) these
cornifications are extended into sharp claws which have a great
resemblance to those of lizards. Claws have been described in
certain fossil Amphibia, but they are undoubtedly a new inven-
tion within the Hynobiidae. Pointed clawlike caps cover the
digit tips of the swamp-dwelling Siren as well as the tips of the
three inner toes of the African pond frogs of the family Pipidae.
The main part of the suction disc on the ventral surface of Stau-
rois tadpoles is covered with tubercles which have a cornified
margin. Most frog tadpoles are provided with a battery of

THE INTEGUMENT

139

horny teeth which function as rasping organs (Fig. 54). Some
tree-frog tadpoles which pass their larval life in water basins
formed by the soft leaves of bromeliads exhibit a great reduction
of the teeth, while various plankton feeders among the tadpoles
have no horny teeth at all. Friction is well known to induce
cornifications on the hand of man, but the importance of the
mechanical factor in the development of tadpole teeth is by no
means clear (Noble, 1929).

Fig. 54. — Larval teeth of a Spade-foot Toad. A section of the two tooth-rows
of Scaphiopus holbrookii, showing modification of single cells to produce individual
teeth.

Adult Amphibia frequently produce horny papillae over their
heads or backs. In the males of many frogs and a few salaman-
ders, these papillae may form patches on the thumbs, arms, chest,
or even throat. The evolutionary history of these growths is
discussed above with those of other secondary sexual characters.
The epidermis of metamorphosed Amphibia is provided with a
series of flask cells which hold the horny layer to the underlying
sheets of epidermal cells. At the time of skin shedding they
release a secretion and withdraw from the horny layer (Muhse,
1909; Dennert, 1924). Only the superficial layer of cornified
epidermal cells is shed at this time.

Molt. — Molting occurs periodically in metamorphosed
Amphibia at varying intervals, frequently a month or more apart.
The process may require a few hours or more than a day.

140 THE BIOLOGY OF THE AMPHIBIA

Springer (1909) found in the case of the newt that the greater the
quantity of beef fed the individual the more frequent the
shedding. There may be a relation between the rate of growth
and the number of molts, but in view of the fact that starving
newts also molt the stretching of the epidermis cannot be the
primary cause of molt. Irritating agents frequently induce the
molting of salamanders. Since molting occurs on all surfaces
of the body at one time, even when the irritation is restricted to a
limited area, some mechanism for correlating the simultaneous
action of the flask cells would seem to be present in the skin.
The mechanism once set in action may induce a series of molts in
rapid succession, as Wilder (1925) has shown. Since the number
of cell layers in the epidermis of any one species varies only within
narrow limits, the molting mechanism would seem to induce
cell division in the deeper epidermal layers. Ruzicka (1917)
and Adolph and Collins (1925) have presented evidence that the
correlating mechanism was a chemical one. Since hypophysec-
tomy prevents molting and leads to the development of a thick,
horny layer in both toads and salamanders, molting would seem
to be under hormonal control. The skin shedding of metamor-
phosis is produced by the thyroid hormone (Chap. XIII).
Thyroidectomy of adult newts (Adams and Richards, 1929) has
the same effect as hypophysectomy, namely the piling up of
cornified epidermal layers. Since thyroid grafts in the newt
induce molting while anterior pituitary grafts have no effect
when the thyroid has been removed, it would seem that secretions
of the thyroid play an important part in the normal molting of
this species (Adams, Richards, and Kuder, 1930) and apparently
in Amphibia in general.

Many terrestrial and some aquatic frogs and salamanders eat
the shed skin. The swallowing is begun before the skin is fully
shed and the movements of throat and forelimbs assist in peeling
off the old skin, that of the limbs being turned inside out in the
process.

Skin as a Respiratory Organ. — Aquatic and forest-dwelling
frogs and toads tend to have a smoother skin than species living
in drier situations. There are, however, many exceptions to
this rule, some of the thoroughly aquatic pipid toads having a
rougher skin than many desert bufonids. In general, burrowing
Salientia, such as Scaphiopus, Rhinophrynus, and Cacopus, have
thinner and smoother skins than their epigean relatives. Smooth,

THE INTEGUMENT

141

thin skins undoubtedly facilitate cutaneous respiration, but they
are, of course, more subject to desiccation than thicker, more
cornified ones. Some species of Bufo evaporate water through
their skins as rapidly as Rana (Adolph, 1930), and in no amphib-
ian does the skin retard evaporation to the extent found in the
majority of reptiles.

Amphibia with reduced lungs, and therefore dependent to a
large extent upon cutaneous respiration, have either a very thin
epidermis or have capillaries penetrating it until they assume a
position near the surface. Some frogs during metamorphosis
have a temporary penetration of capillaries into the epidermis to
tide them over this critical period of adjustment to land life
(Maurer, 1898). The Cryptobranchidae have moderately well-
developed lungs but they prefer to use the highly vascular
skin folds of their bodies as veritable gills, for the capillary
diverticula in these folds penetrate almost to the surface of the
thick epidermis and afford ideal conditions for cutaneous respira-
tion. Typhlonectes, the only thoroughly aquatic caecilian,
exhibits a similar vascularization of the epidermis.

Pigmentation. — The Amphibia are often attractively garbed
in colors as bright as those of birds or reptiles. Although diffuse
pigments may occur in the tissue of some Amphibia, most of
their varied colors are produced by different arrangements of three
kinds of pigment cells: the melanophores, the lipophores, and the
guanophores. Black or brown results from a predominance of
melanophores, yellow or red from the lipophores, and white from
the guanophores. Blue and green are produced by various
combinations of these cells.

Colors may be chemical, structural, or a combination of both.
The brilliant green on the back of many tree frogs is due to such a
combination (Fig. 55). The epidermis of the skin from this
region is translucent, acting merely as a protective cover to the
corium with its battery of chromatophores. The lipophores lie
directly under the epidermis and are filled with a yellow, fatty
material in the form of fine drops or granules (Schmidt, 1920).
Beneath the lipophores are the guanophores, cells packed with
crystals of guanine, a substance allied to uric acid. The guano-
phores in turn are underlaid by the melanophores or dark pig-
ment cells. When light falls upon the skin, it makes it appear
green, for the rays of short wave length are reflected back by the
crystals of guanine, those of greater length being absorbed by the

142

THE BIOLOGY OF THE AMPHIBIA

black background of melanophores. The guanophores, if freed

of their lipophore cover,
would appear blue for the
same reason that the sky
appears blue, namely because
of the diffraction of light by
small suspended particles.
The rays at the blue end
of the spectrum are more
scattered than the rays of
greater length. The scatter-
ed rays include not only
blue but also some green,
indigo, and violet. In pass-
ing back through the yellow
color screen formed by the
lipophores, the blue, indigo,
and violet rays are absorbed
and the green alone allowed
to pass. Frogs thus appear
green because, of the light
which falls upon their skin,
only the green rays escape
absorption.

Blue is a rare color in
Amphibia but it occurs as a
variation in Rana clamitans
and normally in various other
frogs. It is due to the same
mechanism as green except
that the lipophores are absent
and the short blue, with some
green, indigo, and violet rays,
are reflected without the
yellow screen to modify the
result.

Red is also not a common
color in Amphibia. Red
and yellow pigments are
very closely allied and are
produced by the same cell,

Fig. 55. — Diagrammatic section of
the skin of a tree frog during color
change. A. Bright green. The lipo-
phores are arranged over the guano-
phores and the melanophores are
partly expanded. B. Dark green. The
guanophores are cylindrical and are
nearly surrounded by the melanophores.
C. Lemon yellow. Lipophores and
guanophores irregularly arranged and
the melanophores are greatly con-
tracted. D. Gray. The lipophores are
greatly flattened and some are squeezed
between the guanophores. The latter
are completely surrounded by the
melanophores. Ep., epidermis; Gu.,
guanophores; Li., lipophores; Me.,
melanophores. {After Schmidt.)

THE INTEGUMENT

143

the lipophore. Some specimens of Salamandra salamandra
or Amby stoma maculatum may possess red instead of the usual
yellow spots, for within a single individual some lipophores may
assume a red tone without any change occurring in the others.
There is, however, an alcohol-insoluble red pigment in the skin
of some frogs (Ballowitz, 1930.) which may prove to be chemically
different from the pigment of lipophores. Cells which bear this
pigment, so-called "allophores," are found also in fish and
reptiles and may possibly represent a fourth type of pigment cell.
The red specimens of Wood Frog and the yellow Triturus cristatus
which have been found in nature owe their color apparently to an
inherited defect in melanophore production. A more complete
failure to develop pigment leads to albinism, reported in many
different groups of Amphibia.

Color Change. — Many tree frogs rival the chameleons in their
ability to change their color rapidly. Such changes are induced

Fig. 56. — Melanophores of a frog, Rana temporaries, expanded (A) and
contracted (B). The processes are not contracted but the pigment is withdrawn
into the body of the cell. (After Hewer, Proc. Roy. Soc. London, 1923.)

by alterations of the form of the chromatophores or plastic pig-
ment cells (Fig. 56). When the green skin darkens, the melano-
phores stream pigment into fine processes which extend between
and around the guanophores. It has been frequently claimed
that no such processes exist in the contracted melanophore but
that the cell extends pseudopodia filled with pigment into preex-
isting spaces between the guanophores and lipophores. Although
the young melanophore in the developing frog or salamander may
change its shape, Amoeba fashion, as it migrates, with advancing
age the melanophore apparently loses this activity until nothing
remains but streaming movements within the extended pseudo-

144 THE BIOLOGY OF THE AMPHIBIA

podia. It seems clear from the work of Schmidt (1919), Sch-
nakenbeck (1922), and others that a darkening is produced by a
migration of pigmented cytoplasm within the mature melano-
phore and that fine, unpigmented processes are maintained even
in the contracted melanophore. When the melanin has reached
its furthest extension, the skin of this region appears black.
In areas where the melanophores are numerous and crowded
closely together, a permanent black spot is produced. We may,
therefore, distinguish between pigment patterns due to the
localization of pigment cells and pigment tones or rarely patterns
due to the change in shape of the pigment cells under various
external or internal influences.

Many tree frogs can change from green to yellow; the melano-
phores become fully contracted and fail to give the guanophores
the necessary black background to permit them to show any con-
siderable amount of blue. The lipophores change their relative
position apparently by amoeboid movement (Schmidt, 1920)
until they lie between, and in a few instances even below,
the guanophores. The yellow rays reflected from the lipophores
are more numerous than the blue from the guanophores, and
the skin appears yellow. Intermediate tones between yellow
and green are produced according to the degree to which
the guanophores function, while color tones between yellow and
dark brown are brought about by an extension of the melanin
in the melanophores. In the absence or feeble development of
the lipophores, the color may vary from gray through bluish to
black. Individuals frequently vary in the development of the
lipophores. Thus, some specimens of Hyla versicolor readily
change from green to nearly black, while others vary from ash
gray to nearly the same tone without being able to assume the
green color. Most Amphibia can darken or lighten their general
body tone but few have the ability to undergo the rapid changes
of color found in some tree frogs. When the guanophores and
lipophores are branched, as in Rana esculenta (Schmidt, 1921), the
color is more diffuse.

Color change is induced by a great variety of factors, both
external and internal. Low temperature in most Amphibia
causes an expansion of the melanophores and hence a darkening
of the skin; high temperatures induce a contraction, and a lighten-
ing. Desiccation and increased illumination have the same effect
as high temperature, while humidity and darkness produce the

THE INTEGUMENT

145

opposite results. In some Amphibia, such as the South American
frog, Leptodactylus ocellatus, the effect of light is induced through
the intermediary of the eyes, for blinded animals fail to respond
to increased illumination (Houssay and Ungar, 1925). In
Rana pipiens the eyes of both tadpole and adult are the chief
receptors of light stimuli affecting the coloration, but, in addition,
the skin responds directly to the stimulation of light (Kropp,
1927), as in some lizards. In the urodeles the importance of the
eye in color change varies with the species and with age. In
very young Ambystoma larvae, as well as in Necturus of all ages,
the skin darkens in the light and pales in the dark. With increas-
ing age in Ambystoma larvae, and hence with increasing function
of the eyes, the reverse change in coloration occurs on exposure
to light on an indifferent background. Blinded larvae of this
age react as young larvae (Laurens, 1917). Salamander larvae
reared in aquaria with dark bottoms develop a dark coloration,
because their eyes, like those of most vertebrates capable of color
change, bring about an expansion of the melanophores. The
impulses originate in the darkened retinae and are so strong that
they overcome the tendency of the darkened chromatophores in
the skin to contract. The tadpoles of Xenopus expand the
melanophores of their tail fin when placed in the dark and appar-
ently because of an optic influence. Seeing black is, however,
very different from being put in darkness, at least in regard to
its effect on the melanophores.

The coloration of the skin of some tree frogs is influenced by
tactile stimulations. The European tree frog turns dark on a
rough surface and green on a smooth surface (Biedermann,
1926). Thus, either the sight or the feel of pale, smooth leaves
may bring an adaptive change in the color. Many Amphibia
both in the field (Hargitt, 1912) and in the laboratory undergo
erratic changes of color which cannot be correlated with any
external factor but are apparently attributable to internal causes.
An insufficient supply of oxygen brings about a contraction of the
melanophores and hence respiratory disturbances would have
some effect on the coloration.

The mechanisms controlling the expansion and contraction
of the pigment cells vary with the species. In some species of
Rana it would seem to be the secretion of the pars intermedia of
the pituitary gland (Smith, 1920; Swingle, 1921) which brings
about an expansion of the melanophores and its absence, a con-

146 THE BIOLOGY OF THE AMPHIBIA

traction. The secretion of the adrenal organs, however, induces a
rapid contraction of the dermal melanophores, although an expan-
sion of the retinal pigment cells, and probably this secretion func-
tions at times of intense excitement. In Rana pipiens, the slow
adaptive responses of the chromatophores have been attributed
to the direct action of light. The very rapid wavelike changes
along the backs of some tree frogs such as H. goughi (Boulenger,
1911) can be due only to nervous mechanisms. Kropp (1927) has
shown that a contraction of the melanophores is produced in
Rana pipiens by nerve section. Hence, while the hormone of the
pars intermedia of the pituitary probably has the most important
part to play in the control of color change, the nervous mecha-
nisms alone can also induce changes and stimuli impinging on the
integument may directly affect the chromatophores without
involving nerves or hormones. It is possible that both hormone
and nerve action may produce the same response, light stimula-
tions received through the eye being transmitted on one hand to
the pituitary and on the other to the nerves in the integument
controlling the form of the melanophores. No doubt the impor-
tance of one or the other mechanism varies with the species.
It is also possible that a third type of influence may originate from
the eye. Kropp (1929) has obtained evidence that a melano-
phore activating substance may be produced by the eye of certain
tadpoles and released directly into the blood stream. Burrowing
or aquatic frogs would not have so great a need for quick changes
of dress as those arboreal species which frequent exposed situa-
tions. Hence the mechanism controlling the chromatophore
expansion would not be expected to be the same in these species.

Color Patterns. — While the ground tone of nearly all Amphibia
is subject to considerable change, the white spots formed by the
accumulations of guanophores and the dark patterns produced
by masses of melanophores change very slowly if at all during
adult life. The patterns have repeated themselves many times
in the evolution of the Amphibia. A dark stripe on the side of
head and body is found in various hynobiids, plethodontids, and
salamandrids; it even appears in the pigmentless cave salamander,
Proteus, when exposed to light (Werner, 1892). Werner showed
that the patterns of the various subspecies of Salamandra sala-
mandra of Europe were repeated in certain species of Oedipus
and Eurycea of the New World. I found that in a few hundred
Desmognathus fuscus carolinensis collected in a single locality,

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147

the patterns of several species in other genera of plethodontids
were represented. The varieties in this collection might have
been arranged to show progressive change in pattern in various
directions, but such series would no doubt not represent the true
order of appearance of these patterns in phylogeny. Many
frogs and toads possess a dark stripe through the eye, extending
beyond the tympanum, and also another between the eyes. The
pattern on the body frequently takes the form of a number of
stripes or rows of spats. Werner (1892) assumes that there were
originally four or six of these stripe areas in the Salientia. Cen-
ters of pigment formation have been described in the skin of
birds and mammals. The number of possible patterns Amphibia
may assume seems limited, for many stripes and bars appear in
the same position in unrelated groups.

A study of the ontogeny of color patterns in urodeles has thrown
some light on the reason for the frequency of the striped pattern
in this group. Linden (1900) found in three species of European
newts that a pattern of longitudinal stripes appeared even before
hatching. The stripes were apparently correlated with the
development of the main blood vessels under the skin. The
longitudinal stripes were in some species gradually changed into
spots, the transformation beginning at the posterior end of the
body and moving forward and spreading from the dorsal surface
to the ventral. There was thus a close parallel between the
ontogeny of the color pattern of these newts and that of the
European lizards, as described in the classical studies of Eimer
(1881).

Eycleshymer (1906) followed the migration of the melano-
phores of Necturus from their origin in the mesenchyme to their
final position in the dermis and epidermis. He noted a tendency
for these pigment cells to aggregate along the large cutaneous
veins. A similar migration and aggregation has been reported
for some of the melanophores of the minnow, Fundulus, by
Stockard (1915); and Zenneck (1894) has noticed the importance
of similar early localizations of pigment in building up the pattern
of a snake. Haecker (1918), from a study of the development of
the melanophores in the axolotl, concluded that pigment was
laid down in centers of active skin growth. It is possible that
skin best supplied with blood might grow fastest. Subsequent
observations (Sluiter, 1920) have not attempted to distinguish
between regions of rapid growth and regions of maximum blood

148

THE BIOLOGY OF THE AMPHIBIA

supply. The striped pattern of many adult salamanders may be
considered a retention of the early larval pattern. In frogs a
somewhat similar pattern may first appear at metamorphosis,
but whether or not it is correlated with regions of active skin
growth has not been determined.

The pigmented sides of many salamander larvae bear three
rows of light spots. In the center of each is usually located a
lateral-line sense organ (Fig. 57). In many plethodontid larvae
the light area is devoid of pigment, but in certain salamandrids
lipophores may be clustered in these areas. In some adult

Fig. 57. — Larva of the two-lined salamander, Eurycea bislineata, showing
the relation of the color pattern to the lateral-line organs. Each small ring within
the light areas represents a lateral-line organ.

salamanders which retain the lateral-line organs, guanophores
may come to occupy the same position. Thus, the lateral-line
organs frequently have an effect on controlling the color pattern,
since melanophores fail to develop near them (Noble, 1927).

Whatever might be the causes of melanophore localization,
it may be noted that melanin is often produced in regions of high
metabolism. The more active hemisphere of frogs eggs is usually
pigmented, although when eggs contain much yolk they may be
devoid of pigmentation. Faris (1924) found that pigment was
produced in the embryo of Ambystoma in regions of rapid dif-
ferentiation rather than of cell proliferation. Melanin is pro-
duced by the oxidation of tyrosin or similar chromogen base,
which is presumably, as in the case of the former, a product of
protein metabolism. The transformation is produced under the
influence of a tyrosinase or similar oxidizing ferment. A tyro-
sinase has been described in the skin of various Amphibia (Ges-
sard, 1904) as well as in the frog's egg.

Banta and Gortner (1913) found that dilute solutions of tyrosin
produced a darkening of the integument of Eurycea bislineata.
Pernitzsch (1913) and Haecker (1918) noted that the difference
between the albino and a pigmented axolotl was not merely a
matter of failure to produce this substance in the albino. They

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149

observed that the melanophores of the albino were smaller and
grew very much more slowly than those of typical specimens.
Pawlas (1925) found, however, that injecting an extract of pig-
mented axolotl skin into an albino axolotl would induce the
development of a pattern. It thus seems that certain parts of
the integument are regions of pigment formation as well as of
accumulation. In many salamanders these regions are the sides
of the body where cutaneous respiration is at a maximum.
Possibly the greater supply of oxygen of the flanks would facilitate
the production of melanin in this area. All patterns are not
correlated with blood vessels. Further, some patterns are
determined before they appear as pigmented areas. Lindeman
(1929) found that transplanting the skin from the back to the
tail of a tadpole before metamorphosis did not prevent the
typical pattern from appearing in this piece of skin at the time
of metamorphosis. Similarly, Reis (1930) found that larval skin
transplanted on a different part of the body of the adult sala-
mander metamorphosed and developed the color pattern it
would have had in its normal position after metamorphosis.
Thus, patterns are determined in the larval skin before there is
any visible accumulation of melanophores. The nature of the
hereditary mechanism determining these patterns has been
discussed in a previous chapter (page 19).

Influence of the Environment on Pigmentation. — Under the
stimulation of light the young of the cave salamanders, Typhlo-
triton and Proteus, will develop an extensive pigmentation of
their integument. On the other hand, densely pigmented larvae,
if reared in the dark, do not necessarily carry any marked effect
of this sojourn into their adult life (Herbst, 1924; Banta, 1912).
Although pattern, as shown from the work of Lindeman and of
Reis, appears to be early localized by hereditary factors, the
degree of development of the color may be influenced in some
cases by light. Herbst and Ascher (1927) showed that the yellow
pigment on the ventral surface of the recently metamorphosed
Salamandra salamandra could be greatly increased by illuminating
the animals from below. It would seem that if salamanders
could expose their ventral surfaces to the light, patterns would
appear which were previously unknown in these species. In
such cases the light would not be producing a new pattern but
merely bringing into view patterns potentially present but not
previously realized because of the lack of light. It would also

150 THE BIOLOGY OF THE AMPHIBIA

seem probable that the degree of pigmentation of the upper sur-
face of a salamander might be a function of the amount of exposure
to light. Babak (1912) found that the increase and spread of
the melanophores were dependent on the form of the cells, the
expanded ones developing more rapidly than the contracted ones.
In the light, Typhlotriton expands its melanophores, while in
the dark, it contracts them. Poorly pigmented tadpoles have
been reported from clay water, and possibly the absence of light
may have hindered their development. Although light is not
necessary for the activation of the tyrosinase reaction, its absence
in certain cases might delay the oxidation.

Pogonowska (1914) found that sodium chloride increased the
formation of black pigment in Salamandra salamandra while it

Fig. 58. — Melanism in salamanders: A. Melanistic specimen of Eurycea melano-
pleura. B. Typical coloration of the same species.

reduced the development of lipophores, and Taniguchi (1929)
has reported a similar effect of common salt on the melanophores
of Hynobius. A mineral mixture added to the diet of beef-
muscle-fed Ambystoma larvae enormously increased the inten-
sity of pigmentation (Patch, in press). Fatty foods may hinder
the development of the black-pigment cells (Johnson, 1913).
Wolterstorff (1927) showed that feeding white worms, Enchy-
traei, to the red-bellied salamander, Triturus pyrrhogaster, would
prevent the red colors from developing. Similarly, Triturus

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151

alpestris reared on Enchytraei and pale copepods develops a white
instead of a yellow abdominal color. Tornier (1907) reported
that Pelobates larvae raised on a meat diet became intensely
dark, in striking contrast to tadpoles of the same species given a
vegetable diet. No doubt some of the color variation found
within a species in nature may be attributed directly to diet.
Field studies have not yet, however, given evidence of such a
correlation. Many herpetologists have reported melanistic
Amphibia (Fig. 58) living side by side with typically colored
individuals of the same species (Werner, 1930). Hence most
melanism is apparently due to genetic and not to environmental
factors. Nevertheless, several external factors are able to influ-
ence the development of pigment. Among these factors are the
type of food the individuals happen to eat. Salts increase
the amount of dark pigmentation, fats decrease it. Further the
amount of light available during ontogeny may have an even
more profound effect on the elaboration of pigment.

The internal environment produced by the hormones has also
an influence on the development of the pigmentation. In the
absence of the pituitary hormone new pigment is not formed
(Peredelsky and Blacher, 1929). Woronzowa (1929) found that
implanting pituitary tissue into the albino race of axolotl would
cause the development of pigment. It is thus evident that the
skin of the white axolotl has potentialities to form normal dark
coloration and that these potentialities may be realized if enough
pituitary hormone is present.

Significance of Color. — The skin screens the underlying tissues
from excessive visible and ultra-violet light by its horny layer and
chiefly by its pigment. A sudden exposure of the stomach of a
frog to ultra-violet rays brings about its contraction (Hill, 1926).
The lipophores, as well as the guanophores and melanophores, act
as a screen (Kruger and Kern, 1924). Many tree frogs, Hyla and
Centronella, with translucent bodies have their viscera well
protected by a covering of guanophores around the peritoneal
cavity, and some tadpoles which habitually swim with their
snouts directly under the surface film are protected by an accumu-
lation of guanophores on the snout (Eggert, 1929). The melano-
phores have an equally important function as heat regulators,
transforming light into heat. The melanophores of the retina
have still another function, permitting rays from only one direc-
tion to reach the sensitive rods and cones, thus increasing

152

THE BIOLOGY OF THE AMPHIBIA

enormously the efficiency of vision. With the marshaling of the
pigment cells into patterns, a further significance was developed,
for frequently such patterns are highly concealing.

The coloration of most Amphibia seems in keeping with their
surroundings. Bright-green tree frogs, such as Hyla andersoni,
remain for long periods on leafy trees; grey ones, such as H.
arenicolor, on rocks. The wood frog, Rana sylvatica, resembles
the brown leaves among which it sometimes hops. The pond-
dwelling ranas usually lack the spots and stripes of those, such as
R. pipiens, which frequent meadows. Nevertheless, it is common
experience to find Amphibia of very different color pattern living
side by side. It is difficult to consider the red color of Pseudo-
triton or the yellow of Eurycea as protective. Rather, these
tints are like those of the leaves in the fall — beautiful but without
value.

Some of the gaudy patterns of Amphibia may be concealing,
functioning according to the well-known camouflage principle of
attracting the attention to them and diverting it away from the
outline of the animal. Thus, the bright, median stripe of some
specimens of Plethodon cinereus or Acris gryllus may assist in the
concealing process. But, one naturally asks, if these stripes are
of such importance, why do not all specimens of these species have
them? In Ambystoma, many species (maculatum, opacum,
annulatum, etc.) are brightly marked, but others in the genus
which seem to have the same habits (jeffersonianum, texanum,
etc.) lack the bright spots. Still others, as A. tigrinum, differ in
both brightness and size of the markings in specimens from
different parts of the continent. Hence, the importance of these
patterns as protective devices seems not extensive.

A number of Salientia have specialized in developing bright
colors on their groins, thighs, or other surfaces which are concealed
by the legs when the frog is at rest. It has been assumed that
the sudden flashing of these colors at the moment of leaping would
dazzle the pursuer. Familiar examples of such " flash colors"
are found on the thighs of Hyla versicolor, the groins of various
species of Dendrobates or Phyllobates. A priori, these would
seem to afford some of the best cases of protective colora-
tion, but field observations as to their dazzling ability are lacking.

A number of Salientia, particularly South American bufonids
and certain brevicipitids, have eyelike spots on the groins (Fig.
59). These have been assumed to function, as the ocelli in the

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153

wings of certain butterflies, in attracting the attention of the
enemy toward them and away from the more essential head
region of the frog. Such speculations afford interesting hypothe-
ses to be critically studied by field students. All the intermedi-
ates between eyelike spots and black inguinal blotches exist
among these frogs. The frequency with which these eye spots
are repeated in unrelated groups gives the impression that they
must have some important,
even though still unknown,
function.

Parallelism in the develop-
ment of color pattern is a
frequent phenomenon in
Amphibia. Plethodon glutin-
osus and Amby stoma jefferson-
ianum resemble each other so
closely that they are often
confused. Various species of
Hyla, Polypedates, and
Leptopelis have almost iden-
tical patterns. If convergent
evolution due to mimicry is
assumed to account for the

first-mentioned Species One tipus ocellatus resembles a face directed
. - , , . ' posteriorly. Eye spots occur in various

might ask Why does the Same unrelated groups of Salientia.

pattern appear in Aneides

flavipunctatus of the West Coast. It seems far more likely that
the integument of Amphibia is limited in the number of possible
patterns which it is able to assume and hence the repetition of
various patterns during evolution.

It has been sometimes assumed that color patterns serve as
recognition marks in the various groups of vertebrates. As most
Amphibia lead solitary lives except during the breeding season,
such marks would function only during a short period. The
bright colors of the males of some newts may serve to attract
the attention of the females, but mechanisms other than color
pattern function in sex recognition of most Amphibia.

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THE BIOLOGY OF THE AMPHIBIA

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Shipley, P. G., and G. B. Wislocki, 1915: The histology of the poison
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Sluiter, C. P., 1920: Rhythmical skin-growth and skin-design in amphibians
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Smith, P. E., 1920: The pigmentary growth and endocrine disturbances
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THE INTEGUMENT

157

Springer, A., 1909: A study of growth in the salamander Diemyctylus

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CHAPTER VII

THE RESPIRATORY SYSTEM

Oxygen required by the tissues for their metabolism is supplied
by the blood. A constant refurnishing of the haemoglobin with
oxygen is demanded if the animal is to live, for cessation of
oxidation results in an accumulation of carbonic, lactic, and other
acids in the tissues, paralyzing and eventually killing the cells.
Carbon dioxide, which in solution gives carbonic acid, is the chief
product of oxidation in the tissues. Since the concentration of
carbon dioxide is greater in the tissues than in the blood, while
that of oxygen is less, an interchange of these gases occurs by
diffusion. The aeration of the blood is described as external
respiration; the exchange of gases between blood and cells is
distinguished by the term "internal respiration."

Since an absorption of oxygen by the blood, as well as the
elimination of carbon dioxide, may occur on almost any part of
the body where a thin, moist membrane overlies a capillary net,
a large part of the integument of Amphibia functions in respira-
tory exchange. In most species the lining of the mouth is very
vascular and serves for buccopharyngeal respiration. The major
role in respiration, however, is played by the gills of the larvae
and by the lungs of the adult. The primitive fish were well
supplied with scales or bony plates in the integument. These,
while affording protection to the animal, tended to limit the
respiratory surface of the body and to necessitate the develop-
ment of gills and lungs as the chief respiratory structures even in
the most primitive forms.

The oxygen and carbon dioxide of the blood are not only in
solution but also in chemical combination which may be readily
broken down to give off the gases. Hence, respiration involves
not only diffusion but also a number of complex chemical trans-
formations. Most of the oxygen is carried in the blood combined
with haemoglobin, while the carbon dioxide is transported
largely in the form of bicarbonates. On the respiratory sur-
faces the haemoglobin in the red blood cells is oxidized to oxy-

158

THE RESPIRATORY SYSTEM

159

haemoglobin, which being more acid than haemoglobin tends to
break up the bicarbonates and drive the carbon dioxide out of
the blood stream. The loss of the carbon dioxide in turn lowers
the acidity of the blood and facilitates the oxidation of the
haemoglobin again. Thus, in the body tissues the accumulation
of carbon dioxide favors the liberation of oxygen from oxyhaemo-
globin by increasing the acidity. Further, the reduction of
oxyhaemoglobin facilitates the taking on of carbon dioxide by
the blood. In short, each chemical transformation on the respira-
tory surfaces or in the deeper tissues favors the one to follow.

Haemoglobin is chemically different in each species of animal.
Its ability to carry and to unload oxygen varies with the species.
The affinity of frog haemoglobin for oxygen is much lower than
that of man. Hence at the same temperature human blood takes
on much more oxygen than frog blood. At the low temperature
ordinarily characteristic of Amphibia (15°C), however, the oxy-
haemoglobin of the frog is able to give up its load of oxygen as
readily as human oxyhaemoglobin will dissociate at a much
higher temperature (37°C; Macela and Seliskar, 1925). In
regard to its affinity for carbon dioxide, the blood of the bullfrog
as compared with mammals binds a comparatively high amount
(Wastl and Seliskar, 1925) but is unable to regulate its alkalinity
as effectively as mammalian blood does.

Gills. — The gills of Amphibia are found only in the larvae and
in those adult urodeles which fail to metamorphose. They
sprout from the side of the neck in the branchial region which is
pierced by a series of clefts. In the Gymnophiona the first cleft
of the series remains open for only a short time during embryonic
life. It forms a spiracle homologous with that of sharks, Polyp-
terus, and a few other fish. In all other Amphibia the entodermal
pouch forming the spiracle never breaks through to the outside
but either produces a Eustachian tube, as in most Salientia, or
disappears. There are four branchial clefts behind this pouch in
most frogs and salamanders, but in the caecilians a fifth also occurs
(Marcus, 1908). This is very probably the retention of a primi-
tive feature, for Edgeworth (1920) has noted the development of
the fifth pouch in the primitive Hynobius and Cryptobranchus.

There early develops in the pharyngeal wall, alternately with
the clefts, a series of cartilaginous bars which form the hyobran-
chial apparatus. The cartilage between spiracle and the first
branchial cleft becomes the hyoid; the following cartilages, the

160

THE BIOLOGY OF THE AMPHIBIA

branchial arches. In caecilians there may be five of these bran-
chial arches in the embryo (Fig. 60), while in all other Amphibia
four is the maximum number and there may be less. The
reduction in the number of arches is not always correlated with
differences in habitat. The brook-dwelling Desmognathus pos-
sesses four branchial arches and some species of Eurycea, three.
Branchial arches have been described in various fossil Amphibia
such as Dwinasaurus, Archegosaurus, and Lysorophus, but they
were not known to be more than four in number. The adult
caecilians have at most four functional branchial arches, and
hence the fifth may never have been a distinct arch in the adults
of any Amphibia.

In the larvae of urodeles and caecilians the gills arise from a
portion of the outer surface of the first three branchial arches.
In the tadpoles of Salientia similar gills appear early in develop-
ment and in some species
they may become greatly
elongated (Chap. III). In
the Marsupial Frog, Gastro-
theca, the two anterior pairs
of external gills may form
enormous bell-shaped struc-
tures which function as vas-
cular wrappings completely
surrounding the embryo. In
most frog tadpoles the exter-
nal gills do not attain the size
or complexity of these struc-
tures in urodeles. Further, they are soon covered over by the
operculum, a fold of integument which grows back from the hyoid
arch. They are then replaced by rows of shorter gill processes,
which grow from the anterior and posterior margins of the same
arches and also from the anterior edge of the fourth branchial arch.
These are often considered internal gills, homologous with the
ordinary gills of fish, in contradistinction to the early formed
gills, which are called " external" and homologized with the
larval gills of crossopterygians and dipnoans. Except for their
point of origin, there is very little difference between external
and internal gills. The tissues entering into their formation are
probably the same (Greil, 1906; Jacobshagen, 1921). Amphibia
have specialized in the elaboration of the external gill which

_b. v.

Fig. 60. — Sagittal section through
the head of the caecilian, Hypogeophis
rostratus, showing the branchial arches
in cross-section. Caecilians are remark-
able in retaining the fifth branchial
arch. B.V., fifth branchial arch; U.,
ultimobranchial body. (After Marcus.)

THE RESPIRATORY SYSTEM

161

was an inheritance from the larvae and not from the adults of
their piscine ancestors.

Relation of Gill Form to Function. — The fully developed form
of the external gills of the various species of Amphibia is closely
correlated with the functional needs of the larvae. This was
shown in the discussion of their life history. The reduction of

Fig. 61. — Head and gill form in Pseudobranchus striatus (A) and Siren lacertina
(B), drawn from living specimens approximately six inches in total length.
Young Siren lacertina (C) after treatment with 1 to 1,000 solution of iodothyrine.
The branchiae are entirely lost, although their position is indicated by a densely
pigmented swelling. Drawn from a formalin-fixed specimen, the lateral-line
organs obscure, not indicated.

the gill clefts may also have a functional significance. For exam-
ple, Siren, with four branchial arches, has the first three clefts
open in the mature animal, while the closely related Pseudo-
branchus, which unlike Siren is a burrowing salamander, has the
same number of arches, but only the second cleft remains open

162 THE BIOLOGY OF THE AMPHIBIA

(Fig. 61). On the other hand, in another burrowing type,
Amphiuma, with four branchial arches and only one cleft, that
between the third and fourth arches, the closure of the arches
may be considered a metamorphic change partly completed.
This seems probable, for Amphiuma shows other metamorphic
changes such as the loss of gills early in larval life, but such an
explanation would not account for the reduction in Pseudo-
branchus (see page 103). Cryptobranchus is another incom-
pletely metamorphosed type which has external gills early in
life and which gives them up without developing internal gills.
The margin of the operculum fuses at the time of gill reduction
to the throat, except at its dorsal end, where a single opening
remains on each side. In Megalobatrachus, which exhibits
further metamorphic changes in its skeleton, the operculum fuses
completely, and this so-called "derotreme" lacks the branchial
fenestrae supposed to characterize the group. No urodele ever
develops internal gills, and salamanders such as Cryptobranchus,
which remain in the water after the external gills are lost, rely to
a considerable extent on their skin for respiration although the
lungs are functional. In other genera such as Necturus, with
two clefts, the reduction may be correlated with the number of
arches formed. This is particularly true of the tadpole of the
Banana Frog, Hoplophryne, which breathes air from the time
of hatching and has only one branchial arch and one cleft on each
side. How many of these instances of reduction can be con-
sidered cases of partial metamorphoses is difficult to decide. In
some species, more arch-forming material seems to be present
from the first.

On the concave side of the branchial arches a series of papillae
develop which are homologous with the gill filters of fish and
which serve the same function, namely, the prevention of the
escape of food through the gill clefts. They seem to have been
bony structures in some branchiosaurs. The short internal
gills of Salientia are protected from the outside by an operculum
as in fish. In the Salientia, however, this is not a bony cover
but merely a fold which grows backward from the hyoid arch
over the gills and fuses with the integument of the abdomen
except for a small opening, the so-called " spiracle," which may
be medial (discoglossids, brevicipitids, etc.) or sinistral (most
Salientia). Rarely there is left a small opening on each side
(pipids). In this way a branchial chamber is formed which

THE RESPIRATORY SYSTEM 163

freely communicates with the one of the opposite side by a broad
channel ventral to the pericardium.

Fig. 62. — Skin capillaries. The efficiency of cutaneous respiration is increased
in the Plethodontidae by the thinning of the epidermis over the superficial
capillaries. In the Cryptobranchidae and certain other salamanders the
capillaries penetrate the epidermis to a position very near the surface. A.
Desmognathus quadra-maculatus . B. Cryptobranchus alleganiensis. Ba.Mbr.,
basal membrane; Cap., capillary; Ep., epidermis; G.La., germinal layer; Hor.La.,
horny layer; M.GL, mucous gland; P.GL, poison gland; Tr.La., transitional layer
of epidermis; Cor., corium.

Integument in Respiration. — The integument of the body of
Amphibia, although it is often highly vascular and has important
respiratory functions, is rarely thrown into processes resembling
gills. The folds along the body of Cryptobranchus are consider-

164

THE BIOLOGY OF THE AMPHIBIA

ably vascularized, the capillaries penetrating almost to the outer
surface of the epidermis (Fig. 62). These folds are often waved
back and forth by the submerged animal in a manner suggesting
the gill movements of such forms as Necturus. Similar body
folds occur in the aquatic Andean frog, Batrachophrynus. The
larva of Xenopus is provided with a pair of long vascular barbels
which have been credited with primarily tactile and not respiratory
functions (Nikitin, 1925). Only in the " Hairy Frog" of Africa,

Fig. 63. — The 'Hairy Frog' Astylosternus robustus receives its name from the
thick growth of vascular villosities which develop in the male during the breeding
season. These are respiratory organs which compensate for the reduced lungs
of this species at the time of the year when the metabolism of frogs increases.

Astylosternus robustus do vascular papillae occur which resemble
the finer branches of gills (Fig. 63). These are found only in
the male and apparently compensate for the greatly reduced
lungs of this frog. Their elaboration during the breeding season
is to be explained by the increased metabolism during this season
and the need for oxygen by the very muscular males. The
villosities which occur on the thighs and flanks resemble those
which develop on the hind limbs of the brooding male, Le pi do-
siren, where they assist this fish to secure sufficient oxygen
without leaving the egg burrow.

Lungs. — Gills and integumental filaments occur only in aquatic
forms. On land the villosities would stick together and would
greatly reduce the respiratory area. Those that remained

THE RESPIRATORY SYSTEM

165

exposed would dry due to the absence of glands and would soon
lose their respiratory function. The respiratory organs of terres-
trial vertebrates are the lungs. These arose in phylogeny long
before the land was invaded. They are found today in both
dipnoans and crossopterygians, and it seems probable that
crossopterygian fish closely allied to the ancestors of Amphibia

Fig. 64. — Frontal section of a larva of the midwife toad, Alytes, showing the
resemblance of the lung rudiments to branchial pouches. L.A., lung anlagen.
Visceral pouches numbered. {After Makuschok.)

had paired air sacs of the same form as lungs (Barrell, 1916).
Further, both air bladders and lungs arise from entodermal
pockets of the pharynx which are serially homologous to the
pockets which break through to form the gill clefts. That lungs
are branchial pouches and not mere intestinal diverticula which
have taken over secondarily a respiratory function is well shown
by their development (Fig. 64) in the more primitive Amphibia
and especially by the Gymnophiona as described by Marcus

166

THE BIOLOGY OF THE AMPHIBIA

(1908, 1922). In the embryo of Hypogeophis, Marcus identifies
nine visceral arches homologous to those in primitive fish. The
first forms the cartilage of the jaws, the second that of the hyoid,
the third to seventh inclusive, the branchial arches, the eighth a
process on the larynx, and the ninth the bulk of this structure.
The entodermal pouch, which pushes out between hyoid and
jawbone, breaks through to the exterior to form the spiracle.
The pouch caudal to the hyoid and those following the first four
branchial arches become gill clefts. That following the fifth
branchial arch becomes the ultimobranchial body, an epithelial
structure to be considered with the endocrine structures, while the
pouch lying caudal to the sixth and before the seventh develops
into lung.

The other Amphibia fail to show as clearly as the caecilians
the origin of lungs from branchial pouches. Further, Edgeworth
(1920) found that the laryngeal muscles of salamanders were
not split off from the branchial muscles, as might be expected
from the conditions in caecilians, but arose from the splanchnic
layer covering the digestive tract. Edgeworth, therefore, sup-
ported the view of Greil and others that the lungs are not
branchial structures. In view of the more primitive arrangement
of the clefts and arches in caecilians, it would seem that the
musculature of the urodele larynx had undergone various
secondary changes.

The lungs of caecilians are specialized in that usually the left
is rudimentary. The same reduction occurs in most snakes and
seems to be correlated with the elongate body form of both groups.
Another convergence occurs in the aquatic Typhlonectes, which
develops a tracheal lung or respiratory area along the passageway
between lung and pharynx as in some snakes (Fuhrmann, 1914).
The inner surface of the lungs of caecilians is divided by a net-
work of blood vessels, connective tissue, and smooth muscle
which form alveoli. In the terrestrial Salientia such as Bufo,
these chambers are small and numerous, and the septa branch,
forming additional chambers (Fig. 65). The septa are highly
vascular and clothed with a thin epithelium except along their
inner edges where ciliate and mucous cells are abundant covering
bundles of smooth muscle. In many aquatic urodeles which
practice extensive cutaneous and buccopharyngeal respiration the
lungs are poorly vascularized and alveoli are not formed. This
is true of some newts and especially the perennibranchs Proteus

THE RESPIRATORY SYSTEM

167

and Necturus. Simplicity of lung structure may be either a
larval feature or a result of secondary degeneration in the
Amphibia; it is not a primitivism.

The same holds true for the fishes which seem to have evolved
poorly vascularized swim bladders out of lungs. As in newts,
these are used as hydrostatic organs but in most teleosts are
further modified in that only one sac develops, and this may
sprout from the dorsal instead of the ventral side of the digestive
tract. The further modification of the swim bladder in teleosts

A B

Fig. 65. — Comparison of the lungs of two Salientia. Ascaphus truei .(.A),
living in cold mountain streams, relies chiefly on cutaneous respiration, and its
lungs are greatly reduced both in size and in vascularity. Bufo marinus (B),
being terrestrial and having a thick epidermis, has need of large, well-vascularized
lungs. In A only the left lung is shown and this is greatly enlarged. In B the
right lung is open to show the alveolar structure of its inner surface (after Marcus).

is very extensive and has no parallel in Amphibia, excepting in
the case of its reduction and loss.

Salamanders are the only vertebrates above the fish which
have succeeded in dispensing with their lungs. All plethodontids
lack lungs, and various ambystomids and salamandrids exhibit
reductions which lead to rudiments only 5 mm. long in Rhyaco-
triton and 2 mm. in Salamandrina. All Amphibia practice
cutaneous respiration and most of them buccopharyngeal respira-
tion in either the air or water. Still, the lungs have not merely
dwindled away because other respiratory systems were function-
ing. The lungs when well developed act as hydrostatic organs,
and hence no salamanders inhabiti monguntain brooks, where

168

THE BIOLOGY OF THE AMPHIBIA

there would be frequent need of hiding under rocks to avoid the
current, have the lungs so extensive as typical pond species. A
parallel reduction occurs in the swim bladders of mountain-brook
fish. The water of mountain brooks being cool, well-oxygenated,
and running gives maximum possibilities for cutaneous respira-
tion. Nevertheless, in all Amphibia which undergo a reduction
of the lungs, the capillaries either penetrate into the epidermis to
facilitate cutaneous respiration or the epidermis remains thin
over the superficial skin capillaries (Noble, 1925). The cool,
wet crannies along the banks of streams afford an ideal situation
for cutaneous respiration on land, since gas interchange can take
place only if the skin is moist. This habitat was invaded by
plethodontids which had evolved from stream-dwelling sala-
mandrids. The ancestral plethodontids had apparently already
lost their lungs, as modern species show at most the barest
indication of a lung vestige during development (Mekeel, 1926).
Other salamanders, by increasing the efficiency of cutaneous
respiration in the same way as stream salamanders, were able to
survive with reduced lungs in suitable situations without ever
having gone through a typical stream life in the course of their
phylogeny. This is highly probable in the case of Salamandrina
and the European Alpine Salamander, Salamandra atra. Cold,
by slowing down metabolism, reduces the need for oxygen.
Hence, frogs can survive under water for long periods at low
temperatures but will quickly die if the temperature is raised.
Cold seems to have been an important factor in permitting lung
reduction in Ascaphus (Fig. 65A), since other stream-dwelling
frogs in warmer waters have larger lungs. There are thus
various factors which have made possible the reduction and loss
of lungs in Amphibia (Noble, 1929). In the fishes, also, the
hydrostatic organ was lost under a variety of conditions.

Larynx. — The lungs of Amphibia arise from a median evagina-
tion from the ventral wall of the pharynx. This becomes the
laryngeal sac which opens by the glottis into the pharynx. It is
very short in most Salientia, but in the Pipidae, where the lungs
are important hydrostatic organs, the sac is carried posteriorly
to form a trachea and this again divides into two tubes, the
bronchi, which finally lead to the lungs. Pipa is further remark-
able in showing a very complete infiltration of the lungs by
cartilage. This strengthens the septa and other supporting
structures and even forms projections extending into the lumen

THE RESPIRATORY SYSTEM 169

(Marcus, 1927). Cranially the cartilages tend to form rings or
plates which support the bronchial tubes and trachea. The
caecilians, also, exhibit an infiltration of the lungs by cartilage
(Marcus, 1927), which may, therefore, be a primitive feature of
the Amphibia. The urodeles, in correlation with their elongate
body form, usually possess a distinct trachea. This is longest
in Amphiuma and Siren, which possess tracheal cartilages
homologous with those of caecilians. The cartilages which
support the larynx have a differ- ^-L. o.

Fig. 66. — Laryngeal cartilages of a Fig. 67. — Vocal cords of male Bull-
Spade-foot Toad, Scaphiopus holbrookii, frog, Rana catesbeiana; sagittal section of
viewed from the right side. Ary., the larynx viewed from within. Car. H.,
arytenoid; Cric, cricoid; P.P., pul- cartilaginous body of hyoid; I.L., inferior
monary process. vocal ligament; L., left lung; L.O.,

laryngeal orifice; P.P., pulmonary proc-
ess of cricoid; S.L., superior vocal
ligament.

any cartilage in the pulmonary structures. As discussed above,
the laryngeal cartilages arise from the branchial arches, the sixth
and seventh, i.e., the eighth and ninth visceral, being the arches
in caecilians and apparently also in other Amphibia, taking
part in their formation. The last arch, which is much the larger,
forms a cartilaginous bar on each side of the larynx. This may
fuse in caecilians above the larynx with its mate of the opposite
side. In most urodeles and all frogs the cartilage of each side
splits into an anterior arytenoid and a posterior cricoid cartilage.
In the Salientia the arytenoids usually form a pair of spoon-
shaped cartilages lying in a narrow ring, the cricoids, which may

170

THE BIOLOGY OF THE AMPHIBIA

or may not be fused (Fig. 66). These lie between the thyroid
processes of the hyoid and usually send a pair of hook-shaped
processes around the bases of the lungs (Fig. 67). In some frogs
the tips of the hooks may be fused in the midline tending to
obscure further the original bilateral origin of the laryngeal
cartilages. The more anterior pair of branchial bars which take
part in the formation of the skeleton of the larynx have been
shown by Marcus (1922) to form merely a pair of processes on
the arytenoids. The latter guard the entrance to the trachea
and are moved by a dilator and usually several constrictor
muscles.

In the Salientia the laryngeal chamber is divided into two
parts by the vocal organs. These have the form of two thickened
lips which extend across the passageway. They represent exten-
sions of the tissue lining the arytenoids. Each lip may be
divided by a groove in some frogs into an outer and an inner
rim. The vocal cords are formed by the latter. Air forced from
the lungs sets the elastic inner rim of each vocal organ vibrating
and the sound is reinforced by resonating sacs lying either in the
floor or at each corner of the mouth. The air is forced back and
forth between vocal sacs and lungs, usually very little additional
air being taken in through the nostrils. The vocal sacs are
formed by diverticula of the lining of the mouth. Since they
usually lie just above the subhyoid muscle, they force the air
back into the lungs chiefly by the action of this muscle. In
many species the diverticula fuse in the midline to form a median
throat sac capable of great distention. It is because the vocal
mechanism represents a closed system that frogs can call when
under water. The larynx is usually very much larger in the
male than the female, and the latter lacks vocal pouches. As
there is no true larynx at all in fishes, the Amphibia have made a
considerable advance not only in the development of this struc-
ture with its cartilages but also in producing a trachea and
bronchus including their cartilaginous skeleton.

Ways of Respiration. — The Amphibia possess several respira-
tory mechanisms. These, however, are not available to all
species, and, further, a complication occurs in that the mecha-
nisms' of the larva are usually replaced by others during adult
life. The ontogenetic sequence of mechanisms shows little
relation to the phylogenetic sequence, except in the case of the
perennibranchs which have retained or elaborated the larval

THE RESPIRATORY SYSTEM

111

organization. In the larvae of the more primitive salamanders
such as the newt, movements of the branchial apparatus bring
water in through the nostrils and out through the gill clefts,
but in some species cilia play an important part in maintaining
this respiratory current. The external gills are equipped with
muscles which give them independent though limited motion.
The lower jaw also functions as a force pump driving water
from the partly open mouth out through the clefts or nares. The
same mechanism is found in tadpoles except that the gills are
covered by an operculum and are devoid of muscles. Many
tadpoles and urodele larvae increase the efficiency of this appara-
tus by developing valves about the internal nares; these prevent
a backflow of water through the nasal chamber. Since the
buccal cavity is highly vascular in larval Amphibia, some gaseous
exchange takes place through the walls. Most larvae enjoy not
only branchial but also some buccopharyngeal and cutaneous
respiration in the water. As the larvae develop they rise to the
surface and snap for air. The air bubbles function in the gaseous
exchange within the buccal cavity. In many salamanders and
frogs the lungs become functional during larval life and the air
bubble snatched from the surface is pressed back through the
glottis into the lungs. Some tadpoles, however, such as those of
Bufo may fail to develop functional lungs until after metamor-
phosis has occurred. Some urodele larvae respond quickly to
lack of oxygen by increased respiratory movements (Babak, 1921)
and hence must have well-developed nervous centers of respira-
tory control, analogous, if not homologous, to those of higher
vertebrates. There is considerable variation in the respiratory
mechanisms of the various species of Amphibia, but primitively
the larvae would seem to practice buccopharyngeal, pulmonary,
and cutaneous respiration.

Urodeles and Salientia lose their gills on metamorphosis but
the other respiratory mechanisms of the larvae are transmitted
to the adult and further elaborated. In the air the mouth is
held tightly closed. The lips are formed to fit firmly together
and in some species a muscle is developed in the upper lip assuring
by its tension a close union of the jaws (Bruner, 1902). Air is
sucked in and forced out of the nares by a rhythmical lowering
of the floor of the mouth. Smooth muscles develop about the
external nares of the metamorphosed urodele better to control
the respiratory currents. There are two dilators and a con-

172

THE BIOLOGY OF THE AMPHIBIA

strictor. Bruner (1896) has shown that the latter contracts
whenever the nostrils are moistened. In the water the nares
are closed but most urodeles in this situation resume their larval
habits of buccopharyngeal respiration and water is taken in and
expelled from the mouth.

Apparently the smooth muscle equipment of the external nares
was found inadequate for the needs of the Salientia, and they
seized upon a unique way of utilizing the quick-moving striated
jaw and throat muscles for effecting a closing of the nares. A
tubercle was formed on the anterior angle of the lower jaw and
this, supported by the small mento-Meckelian bones underlying
it, was made available as a wedge. When, either by a contraction
of the submental muscle or by a slight
forward movement of the lower jaw, the
tubercle is carried upward, it pushes apart
the two premaxillary bones and this in
turn effects a closing of the nostrils by
carrying mesially the prenasal superior
process of the nasal cartilage (Gaupp,
1896). Though rudimentary smooth
Fig. 68.— a secondary muscles of the urodele nares are present
mechanism for closing the in Salientia, they apparently play no

nasal chamber of frogs. ' J j r J

Roof of the mouth of Rana part in the occlusion of the nostril (Bruner,
escuienta on which is ache- 1902), except in such forms as Xenopus

matically projected the <•

hyoid and the anterior having fused premaxillaries.

end of the omosternum. In both urodeles and Salientia the

A process of the hyoid fits

into the internal nares rhythmical throat movements of buc-
^After ^wuurn^ raised* copharyngeal respiration are interrupted
by a deeper lowering of the throat. At
the height of this movement the nares are closed, the glottis
opened, and the air streams from the lungs into the buccal
cavity. Immediately the throat muscles are vigorously con-
tracted and the mixed air is forced back into the lungs
through the open glottis. After one or more of these expira-
tory and inspiratory movements the glottis is closed again,
the nares opened, and the shallower movements of buccopharyn-
geal ventilation continue. There is some specific variation in
the exact moment that the nares are closed. If they are retained
open too long, as in some aquatic salamanders, a secondary
snapping of air is necessary to provide enough air in the bucco-
pharyngeal chamber to fill the lungs properly. The efficiency

THE RESPIRATORY SYSTEM

173

of this mechanism is further increased in some Salientia such as
Pelobates by using the anterior processes of the hyoids as plugs
(Fig. 68) for the internal nares during the period that the lungs
are being emptied and filled (Willem, 1924). Some of these
differences in the respiratory mechanisms of adult Amphibia
would seem to be correlated with habitat differences. Newts
rising to the surface can probably fill their throats more quickly
through the mouth than through the nostrils. Pelobates and
other burrowing Salientia are continually subjecting their
muscles to strains which would make an extra guard on the
respiratory outlets an advantage.

Lunglessness. — The modification of the adult mechanism
reaches its extreme in those urodeles which have reduced or
entirely lost their lungs. The conditions under which these
are lost have been discussed above, and it was noted that in
these forms the efficiency of cutaneous respiration was increased
either by the penetration of capillaries into the epidermis or the
thinning of the epidermis over the superficial capillaries. The
efficiency of buccopharyngeal respiration is increased not only
by a vascularization of the epithelium but also, by an increase
in the rate of the throat movements of buccopharyngeal respira-
tion. These movements in such lungless salamanders as Aneides
lugubris may reach the remarkable rate of 120 to 180 vibrations
a minute (Ritter and Miller, 1899). Some lungless salamanders
such as Pseudotriton ruber are primarily aquatic, and one might
imagine that buccopharyngeal respiration in the water would
be as active as on land. It is surprising to find that this is not
the case and that these species take no water into their mouths
when submerged (Noble, 1925). This is the more unexpected
in that Salamandrina, which has greatly reduced lungs and is
primarily terrestrial, is able to practice aquatic buccopharyngeal
respiration (Bruner, 1896).

The buccopharyngeal respiration of lungless salamanders is
ample proof that this is a distinct mode of respiration taken over
from larval life and not primarily a means of facilitating the flow
of blood in the lungs, as Keith (1904) maintains. The
pulmonary circulation of Amphibia is retarded by the pulmon-
ary pressure which, thanks to the character of the respiratory
apparatus, is always greater than that of the atmosphere.
Nevertheless, this pressure is not detrimental to pulmonary
circulation.

174

THE BIOLOGY OF THE AMPHIBIA

Comparison with Other Vertebrates. — The respiratory mecha-
nisms of the larval Amphibia have considerable structural and
functional resemblance to those of fish, but those of the adult
show little approach to the conditions in other tetrapods. The
reason is to be found in the reduction or loss of the ribs in modern
Amphibia. The respiratory mechanism of reptiles is a suction
apparatus with the ribs pulling the air into the lungs where the
pressure is less than that of the atmosphere and then forcing it
out again. Some fossil Amphibia, having longer ribs than modern
species, may have had the beginnings of this mechanism.

Marcus (1923) sees in the respiration of caecilians a mechanism
intermediate between that of fish and reptiles. This may
represent the primitive inheritance of Amphibia. The ribs do
not function in either inspiration or expiration of caecilians, but
the laryngeal cartilages which are serially homologous to branchial
arches are forced back and pressed together when air is taken into
the glottis in much the same way that branchial arches of the
fish are retracted during a swallowing movement. In frogs and
urodeles there may be also some movement of the larynx in
respiration but in the position of rest the larynx is forward in
caecilians and reptiles while it is backwardly situated in frogs.
The caecilians take air into the buccal cavity as in other Amphibia.
In these forms, however, inspiration includes not only a lifting of
the floor of the mouth but also a backward movement of the
closed glottis. The small mouths of caecilians may be ample
justification for their not elaborating the buccal movements
found in other forms. The laryngeal movements, however, seem
a primitive feature which was handed on with further modifica-
tion to reptiles.

In both fish and amphibians the efficiency of cutaneous respira-
tion is frequently increased by structural changes in the integu-
ment. In any one individual there is a considerable variation
in the respiratory quotient at different times of the year. Dolk
and Postma (1927), in extending the earlier work of Krogh (1910),
have shown that there is an almost constant intake of oxygen
through the skin of frogs throughout the year, a slight rise
occurring only during the spawning season. Further, the skin
releases more carbon dioxide than the lungs and shows consider-
able variation, with the greatest drop occurring in winter. The
oxygen absorption through the lungs varies with the season,
reaching a peak during the breeding period. Krogh (1904, 1910)

THE RESPIRATORY SYSTEM

175

suggested that the rate of oxygen consumption might be depend-
ent on the rate of blood flow through the lungs, which in turn
would be regulated by the vasomotor system. Bastert (1929)
has shown that there exists a vasomotor control over the pul-
monary vascular supply, which, between certain limits, rations
out the oxygen from the lungs and sends a constant supply of
oxygen to the tissues. This mechanism functions only when
the central nervous system is intact. When the central nervous
system is destroyed, the oxygen supply to the tissues varies with
the oxygen pressure and follows the ordinary laws of gas diffusion.
The integument is able to make no such change in oxygen con-
sumption even though the increased metabolism of the breeding
season makes an increased demand for oxygen at this time.
Where increased efficiency of cutaneous respiration is imperative,
for example in species which have reduced their lungs, a change
in the structure of the integument occurs to make this increase
possible. Apparently no regulatory variations are possible here
as in the lungs.

Respiratory Responses. — In salamanders with reduced lungs,
the buccopharyngeal as well as the cutaneous respiration increases
in importance. Lapicque and Pete tin (1910) found that Euproc-
tus immersed in vaseline succumbed in 24 hours, while it remained
normal with its buccal cavity obstructed. Hence, in this species
with reduced lungs, cutaneous respiration is more important than
buccopharyngeal. Probably less aquatic species will show more
dependence on buccopharyngeal respiration, for in these animals
the rate of the throat movements increases. The buccopharyn-
geal movements of frogs are far more regular than their pulmon-
ary movements, which may be suspended entirely as during
hibernation. A change in the rate of the throat movements has
frequently been used as an indication that the frog is aware
of certain sensory stimulations. Sudden illumination, moving
images, mechanical vibrations, spontaneous movements of the
body, temperature change, and various other factors will induce
a change in the rate of the buccopharyngeal respiration of the
frog. Cole and Allison (1929) have shown that higher rates due
to an increase in the illumination or to moving images gradually
decrease to the original rate, indicating an adaptation to the
new conditions. Since blinded frogs do not show such a response,
the eyes, and possibly the photochemical changes in the eyes,
have some relation to these changes.

176

THE BIOLOGY OF THE AMPHIBIA

Popow and Wagner (1928) studied the effect of nutritive fluids
on the pharyngeal movements of the isolated head of the frog.
Increasing the carbon dioxide content of the fluid induced a
marked increase in the respiratory movements. Apparently
the carbon dioxide, by making the blood more acid, increased
the rate of respiration, as it is assumed to do in the intact animal.
The nervous centers controlling the respiration probably involve
several parts of the brain (Chap. XV). Stewart (1923) found
that removing the cerebral hemispheres of Necturus induced an
increased rate of gill movement. Apparently the hemispheres
inhibit the normal gill movements. Impulses from the medulla
by way of the vagus nerves keep the lungs of Cryptobranchus, and
presumably of other salamanders also, in a state of relaxation. A
destruction of the nerve fibers induces a hypertonic state of the
lungs (Luckhardt and Carlson, 1921). The section of the vagus
in reptiles seems to have the opposite effect, but in these animals
the vagus control has not been adequately investigated. Appar-
ently these sharply contrasted methods of nervous control of
the lungs in reptiles and modern Amphibia are correlated with
their different methods of respiration.

References

Babak, E., 1921: Die Mechanik und Innervation der Atmung, Winterstein's

"Handb. vergl. Physiol." Pt. 2, 706-810.
Barrell, J., 1916: Influence of Silurian and Devonian climates on the rise

of air-breathing vertebrates, Bull. Geol. Soc. Amer., XXVII, 387-436.
Bastert, C, 1929: Uber die Regulierung des Sauerstoffverbrauches aus der

Lunge der Frosche im Hinblick auf ihr Tauchvermogen, Zeitschr. vergl.

Physiol, IX, 212-218.
Bruner, H. L., 1896: Ein neuer Muskelapparat zum Schliessen und Offnen

der Nasenlocher bei den Salamandriden, Arch. Anat. Physiol., Anat.

Abt, 1896. 395-412, 1 pi.
, 1902: The smooth facial muscles of Anura and Salamandrina, a

contribution to the anatomy and physiology of the respiratory mech-
anism of the amphibians, Morph. Jahrb. XXIX, 317-359, 2 pi.
Cole, W. II., and J. B. Allison, 1929: The pharyngeal breathing rate of the

frog as related to temperature and other factors, Jour. Exp. Zool.,

LIII, 411-420.

Dolk, H. E., and N. Postma, 1927: Uber die Haut- und die Lungenatmung

von Rana temporaria, Zeitschr. vergl. Physiol. V, 417-444.
Edgeworth, F. H., 1920: On the development of the hypobranchial and

laryngeal muscles in Amphibia, Jour. Anat., LIV, 125-162, 15 pis.
Ekman, G., 1913: Experimen telle Untersuchungen uber die Entwicklung

der Kiemenregion (Kiemenfaden und Kiemenspalten) einiger anuren

Amphibien, Morph. Jahrb., XLVII, 419-452.

THE RESPIRATORY SYSTEM

177

Fuhrmann, O., 1914: Le genre Typhlonectes, Neuchdtel Mem. Soc. Sci.
Nat., V, 112-138.

Gatjpp, E., 1896: Zur Lehre von dem Athmungsmechanismus beim Frosch,

Arch. Anat. Physiol, Anat. AM., 1896, 239-268.
Greil, A., 1906: Tiber die Homologie der Anamnierkiemen. Anat. Anz.,

XXVIII, 256-272.

Harrison, Ross G., 1921: Experiments on the development of the gills

in the amphibian embryo, Biol. Bull. XLI, 156-170.
Jacobshagen, E., 1921 : Die Homologie der Wirbeltierkiemen, Jena. Zeitschr.,

LVII, 87-142, 2 pis.
Keith, A., 1904: Respiration in Frogs, Nature, LXIX, 511-512.
Krogh, A., 1904: On the cutaneous and pulmonary respiration of the frog,

Skand. Arch. Physiol., XV, 328.
, 1910: On the mechanism of the gas exchange in the lungs, Skand.

Arch. Physiol, XXIII, 248.
Lapicque, L., et J. Petetin, 1910: Sur la respiration d'un batracien urodele

sans poumons, Euproctus montanus, Compt. rend. Soc. Biol, LXIX,

84-86.

Luckhardt, A. B., and A. J. Carlson, 1921: Studies on the visceral sensory

nervous system; 6. Lung automatism and lung reflexes in Crypto-

branchus with further notes on the physiology of the lung of Necturus,

Amer. Jour. Physiol, LV, 212-222.
Macela, T., and A. Seliskar, 1925: The influence of temperature on the

equilibrium between oxygen and haemoglobin of various forms of life,

Jour. Physiol, LX, 428-442.
Marcus, H., 1908: Beitrage zur Kenntnis der Gymnophionen; I. tlber

das Schlundspaltengebiet, Arch. Mikr. Anat., LXXI, 695-744, 4 pis.
, 1922: Der Kehlkopf bei Hypogeophis, Anat. Anz. Erghefl, LV,

188-202.

, 1923: Beitrage zur Kenntnis der Gymnophionen; VI. tjber den

Ubergang von der Wasser- zur Luftatmung mit besonderer Beriicksichti-
gung des Atemmechanismus von Hypogeophis, Zeitschr. Anat. Entw.,
LXIX, 328-343.

, 1927: Lungenstudien, Morph. Jahrb., LVIII, 100-121.

Mekeel, A. Grace, 1926: A pulmonary vestige in the lungless salamanders,
Anat. Rec, XXXIV, 141.

Nikitin, B., 1925: Some particularities in the development of the vascular
system of Xenopus, Bull. Soc. Natur. Moscow, Sec. Biol, N. S. XXXIV,
305-308.

Noble, G. K., 1925: The integumentary, pulmonary and cardiac modifica-
tions correlated with increased cutaneous respiration in the Amphibia;
A solution of the "hairy frog" problem, Jour. Morph. Physiol, XL,
341-416.

, 1929: The adaptive modifications of the arboreal tadpoles of Hop-

lophryne and the torrent tadpoles of Staurois, Bull. Amer. Mus. Nat.

Hist., LVIII, Art. VII, 291-334.
Popow, N. A., and L. B. Wagner, 1928: Zur Frage nach dem Einfluss der

Kohlensaure auf das Atmungszentrum des Frosches, Zeitschr. vergl

Physiol, VIII, 89-98.

178

THE BIOLOGY OF THE AMPHIBIA

Ritter, William E., and Loye Miller, 1899: A contribution to the life

history of Autodax lugubris Hallow., a Californian salamander, Amer.

Naturalist, XXXIII, 691-704.
Stewart, G. N., 1923: The gill movements in one of the perennibranchiate

urodela (Necturus maculatus) and their relation to the central nervous

system, Amer. Jour. Physiol., LXVI, 288-296.
Wastl, H., and A. Seliskar, 1925: Observations on the combination of CO2

in the blood of the bullfrog (Rana catesbiana), Jour. Physiol., LX,

264-268.

Willem, L., 1924: Recherches sur la respiration aerienne des amphibiens.
Bull. Acad. Roy. Belgique. CI. Sci., X, 31-47.

CHAPTER VIII

THE CIRCULATORY SYSTEM

Food absorbed by the digestive system is carried by the fluids
of either the blood or lymph channels to all parts of the body.
Blood owes its color to the protein pigment haemoglobin which
is present in the red blood cells. Haemoglobin possesses the
property of absorbing oxygen where it is plentiful and releasing
it again in regions poor in this commodity. The blood, there-
fore, although having important nutritive functions, is the chief
medium for the transportation of oxygen throughout the body.
Lymph differs from blood in lacking the red blood corpuscles
and specializes in feeding and cleansing the tissues of the body.
Blood and lymph also transport the phagocytic cells, which
destroy infectious bacteria and carry away the fragments of cell
decomposition to the organs where they are eliminated. In
brief, the circulatory system carries the materials necessary for
metabolism to the cells of the body and transports the waste
products from them to the excretory organs. It also carries the
hormones, or chemical " messengers," from the endocrine organs
to the body tissues and serves to equilibrate the water content,
thus preventing the rapid drying of exposed parts.

Blood Corpuscles. — The fluid portion of the blood is the plasma.
It contains a high percentage of water, various proteins, salts,
sugars, and fats as well as oxygen and the products of metabolism.
The cellular elements of the circulating blood include the ery-
throcytes or red cells, the thrombocytes or spindle cells, the
leucocytes or white cells. The latter includes the lymphocytes,
the monocytes, and three categories of granulocytes. Of special
interest in Amphibia are the plasmocytes resulting from the
fragmentation of the red blood cells and hence not considered an
additional type. The plasma of Amphibia, on account of the
low body temperature, is a far more efficient carrier of oxygen
than that of mammals (Barcroft, 1924), since more oxygen goes
into solution at lower temperatures. Nevertheless, most of the
oxygen needed by the tissues is brought to them by the

179

180

THE BIOLOGY OF THE AMPHIBIA

erythrocytes. The efficiency of the haemoglobin as a carrier
of oxygen varies with the species due to chemical differences
in their haemoglobin (Chap. VII).

The red blood cell of Amphibia is an elliptical disc sometimes
bulging in the center where the oval nucleus occurs (Fig. 69A).
It varies in size from approximately 70 microns for the greatest
diameter in Amphiuma to 18 microns in Bombina (Ponder, 1924).
Amphiuma may claim the distinction of having the largest
erythrocytes of any animal. Those of some other perennibranchs
are only 7 or 10 microns smaller. This difference between the
size of the erythrocytes of perennibranchs and those of other

ABC D E

Fig. 69. — The principal types of blood cells in the frog, Rana pipiens. A.

Normal erythrocyte. B. Small lymphocyte. C. Eosinophilic leucocyte. D.
Polymorphonuclear leucocyte. E. Thrombocyte. {After Jordan.)

Amphibia extends to all the cells of their bodies and, from observa-
tions of Smith (1925), would seem to be closely correlated with
the lower metabolic rate of these forms. The number of ery-
throcytes varies from nearly 700,000 per cubic millimeter in
Hyla arborea (Heesen, 1924) to 56,633 in Necturus and 36,000
in Proteus (Ponder, 1924). In any species the number is subject
to considerable variation, it being greatest just before spawning
and lowest just after sexual activity. Aquatic forms tend to
have a lower count than terrestrial forms (Heesen, 1924). This
occurs apparently because the blood of aquatic forms is more
subject to dilution. Food, temperature, and disease affect the
number, and there is also a pronounced sexual difference in some
species at least, the male having the greater number of erythrocy-
tes. In case of the frog, the life of any one erythrocyte is
probably not over 100 days (Jordan and Speidel, 1925).
Nevertheless, this is considerably longer than in higher forms. In
man the average life of an erythrocyte is 10 days. The red blood
cells are removed from the blood stream by the liver and spleen,
especially by the Kupffer cells in the former organ. These cells

THE CIRCULATORY SYSTEM

181

protrude into the blood vessels and capture passing erythrocytes
before they disintegrate.

In higher vertebrates there is found both an increase in number
of erythrocytes over that of Amphibia and a diminution in their
size. There is also an increase in the amount of blood as com-
pared with the living weight (Frase, 1930). The smaller the
red blood cell the greater is the surface of exposure in any
quantity of blood. The nucleus, which has nothing to do with
the absorption of oxygen, is finally eliminated in the mammals,
and the Amphibia are noteworthy in showing at various stages a
similar progressive change. In terrestrial Salientia and Caudata

Fig. 70. — Optical section of a blood vessel of Batrachoseps showing enucleated
erythrocytes and basophilic plastids. Ba., basophilic plastids; E.E., enucleated
erythrocytes. {After Emmel.)

as well as in some aquatic forms, there is a fragmentation or
enucleation of some of the red blood cells. In Rana temporaria
this fragmentation has the appearance of the splitting off of
small portions of the cytoplasm (Beyer, 1921). In Bufo the
fragmented portions are larger, while in Bombina they may be
larger than the nucleated portion. In some urodeles there is
so little cytoplasm remaining with the nucleus that the latter
has the appearance of being extruded from the cells as in the
development of erythrocytes in the mammalian embryo. The
fragmentation reaches its extreme in Batrachoseps (Fig. 70)
where more than 90 per cent of the red blood cells are enucleated

182

THE BIOLOGY OF THE AMPHIBIA

(Emmel, 1924). Further, all stages of enucleation may be found
in the circulating blood. This change is not correlated merely
with terrestrialism. Aneides lugubris and Plethodon cinereus
have only 2.3 per cent of the blood so altered. The difference
occurs in both the adults and the embryos, and Emmel has sug-
gested that the great increase of enucleated red blood cells in
Batrachoseps has been conditioned by the abbreviation of the
gills of the embryo and the reduced vascularity of the integument
of the adult. It may well be, however, that the change in the
respiratory efficiency of the blood of Batrachoseps preceded the
alteration of gill form, for an hypertrophy of the gills may be
readily effected during the ontogeny of many urodeles by merely
decreasing the available oxygen (Drastich, 1925).

The thrombocytes or spindle cells resemble erythrocytes but
are smaller and have pointed ends, a granular endoplasm, and
clear ectoplasm (Fig. 69E). They are very unstable and when
brought in contact with foreign substances break down, releasing
a substance which acts on certain plasma proteins in the presence
of blood calcium to form an insoluble clot or coagulation. In
this process the insoluble fibrin is formed from the protein
fibrinogen and blood corpuscles become entangled in the
resulting gel to form the clot. In many lungless salamanders and
especially in Batrachoseps, the thrombocytes are frequently
fragmented and resemble the blood platelets of mammals both
structurally and functionally (Emmel, 1925). There are also
present in Batrachoseps basophilic plasmocytes arising from
basophilic leucocytes. Spindle cells do not occur in mammals,
and the blood platelets which are so important in preventing
excessive bleeding arise from a different type of mother cell.

Phagocytosis. — The lymphocytes, monocytes, and granulocytes
are less abundant in the blood than the erythrocytes and throm-
bocytes. Further, they vary much more in size and form. The
lymphocytes are nucleated blood cells with a large nucleus and a
comparatively small amount of non-granular cytoplasm. The
small lymphocytes are often found associated with rapidly
growing tissues and it has been suggested that they may have
growth stimulating properties (Jordan and Speidel, 1923). The
large lymphocytes specialized for phagocytosis are called " mono-
cytes." The so-called " macrophages, " cells which wander by
amoeboid movement through the tissues, devouring bacteria,
cell debris, or other injurious material, are merely enlarged mono-

THE CIRCULATORY SYSTEM

183

cytes in action outside the blood stream. By injecting cream
into the living tadpole's tail, Clark and Clark (1928) witnessed
the migration of monocytes through capillary walls to phagocy-
tose the fat globules. They get out of the capillaries by squeezing
their way between the epithelial cells of the capillary wall. The
injection of bacteria causes an increase in the monocytes in the
blood, and Pentimalli (1909) concluded that the amphibian
normally responds to bacterial infection by increasing the
production of monocytes.

Some of the granulocytes also have phagocytic functions. The
neutrophiles, which have a finely granular cytoplasm unlike
the other leucocytes, induce the breakdown of worn tissue, while
the macrophages carry away the debris. The eosinophiles (Fig.
69 C), which may be identified by their large eosin-staining gran-
ules, are found commonly along the digestive tract and may have
functions similar to the neutrophiles. As the granulocytes mature,
their nuclei assume very irregular forms and may even divide
into several parts. Granulocytes, like the monocytes, are not
confined to the blood vessels but may migrate into any of the
tissues of the body or may even make their way carrying their
phagocytosed material to the outside of the body by wandering
out on mucous and epidermal surfaces (Claypole, 1893). Jordan
and Speidel (1923a) suggest that the eosinophiles which pass
through the intestinal epithelium and disintegrate among the
fecal contents of the tract may have an immunizing function
against the intestinal bacteria. Most leucocytes which escape
from the blood vessels are returned to them again by way of
lymphatic vessels.

Origin of Blood Corpuscles. — The blood corpuscles all arise
from a single type of cell indistinguishable from the lymphocyte
of the circulating blood but located for the most part in the kidney
of the tadpoles (Jordan and Speidel, 1923a) and in the spleen of
adult frogs such as Rana pipiens. Only for a short period in the
spring, when the metabolic rate is high, does the bone marrow
form the locus for blood histogenesis as in the case of mammals.
In the more terrestrial Rana temporaria, however, with its
higher metabolism, the bone marrow has the same function
found in mammals (Maximow, 1910). Jordan and Speidel
(1923) suggest that the shift of the primary center of blood cell
formation from the kidney in fish to the bone marrow in mammals
is correlated with an increase in the metabolic rate during phylo-

184

THE BIOLOGY OF THE AMPHIBIA

geny. The Amphibia are of interest in showing during ontogeny
the whole range of possible loci. Some species may have dif-
ferent areas for red blood cell and for granulocyte genesis. Thus,
Jordan and Speidel (1924) found that in the newt the spleen
was the sole organ for erythrocyte and thrombocyte formation,
while the granulocytes were generated in outer portions of the
liver. Since the mother cell is the same in both sites, it would
seem that an environmental factor, possibly different degrees of
vascularization, determined the final form assumed by the blood
cell.

There are various masses of lymphoidal tissue in the bodies of
Amphibia. The more conspicuous are located anterior to the
clavicles of frogs or between skin and muscle near the girdles of
burrowing species. During the spring these produce both lym-
phocytes and leucocytes but appear to store fat at other seasons
(von Braunmiihl, 1926). Accumulations of lymphocytes in the
connective tissue and overlying epithelium of the lingual region
occur in both frogs and urodeles. These may be described as
tonsils (Kingsbury, 1912; Myers, 1928). In the urodeles they
occur in front of the glottis, near the articulation of the jaws and
under the tongue. In the Salientia they are of more variable
occurrence, the sublingual tonsil being the most constant.
They usually do not appear until metamorphosis, although in
Bufo they may develop before metamorphosis is complete. The
Amphibia are the lowest group of vertebrates in which tonsils
occur, the lymphocyte accumulations in the fish being too diffuse
to be called tonsils. In these loci lymphocytes and leucocytes
increase by fission. The amphibian tonsils are, thus, defense
stations from which hosts of phagocytosing cells may be mobolized
for an attack against bacteria or protozoan invaders of mouth
and lungs. Red blood cells of Amphibia are also able to undergo
multiplication in the blood stream by mitosis (Dawson, 1928).

Blood Vessels. — The blood vessels as well as the first blood
cells originate from mesoderm. In large-yolked species such as
Desmognathus, discontinuous thickenings of mesoderm, the blood
islands, join to form the vessels (Hilton 1913). In smaller-yolked
forms as Ambystoma, or even in some large-yolked forms as
Megalobatrachus, the area may be more continuous and ventral
on the yolk. Goss (1928) found that cutting away the blood
island from the ventral surface of Ambystoma embryos did not
prevent the development of the blood vessels but that these grew

THE CIRCULATORY SYSTEM

185

without any red blood cells. Federici (1926) obtained similar
results on removing the median ventral blood island of frog
tadpoles. Hence the blood vessels arise from a different primor-
dium than the erythrocytes. The early embryonic vessels are
formed independently of the molding influence of flowing blood,
but very soon in development the mechanical effect of the cir-
culating fluid becomes evident. Clark (1918) found that destroy-
ing the hearts of tadpoles prevented a development of the vessels
beyond an embryonic stage. It would seem that the full elabora-
tion of the blood vessels may be a functional matter dependent
chiefly on the blood pressure within and the available space
without the vessels. In Ambystoma the early differentiation of
brain and pronephros seems to stimulate the development of the
vascular system in these regions at this stage, the chief function
of the vessels being the elimination of injurious products of metab-
olism (Moore, 1915). Nevertheless, the larger vessels continue
to develop according to a definite plan whatever be the mechanical
factors regulating this scheme.

The larger blood vessels of the urodele embryo follow closely
the primitive vertebrate plan. There is a subintestinal vessel
which may be divided anteriorly by the yolk into twoomphalo-
mesenterics. A cardinal vein appears on each side in the body
wall associated with each pronephros and grows posteriorly to
send branches to the caudal or posterior extension of the subin-
testinal vessel (Grodzinski, 1924). At its anterior end the sub-
intestinal sends a series of vessels around the gut between the
gill slits. These join on each side and after uniting to form a
single vessel are continued posteriorly as the dorsal aorta. The
latter gives off intersegmental branches to the body wall and
others supply the gut. The heart, which develops very early in
the subintestinal vessel, pumps the blood through the aortic
arches (the vessels between the gill slits) and back along the dorsal
aorta to supply body wall and gut. The circuit is completed
along the gut by way of the subintestinal vessel and along the
body wall by the postcardinals. The cardinals extend across the
body cavity to form the ducti Cuvierii entering the heart on each
side. The subintestinal is further modified by the growth of
the liver which develops as a glandular outgrowth across the path
of the vessel.

The veins which arise out of this ground plan of embryonic
vessels are the conduits leading blood to the heart. They are

186

THE BIOLOGY OF THE AMPHIBIA

equipped with valves which prevent the backflow of the blood.
The arrangement in urodeles is very similar to that of lung fishes,
and here functional covergence may have produced the structural
resemblance. The post cardinals are present in the larvae of
urodeles and frogs but are usually replaced in the adult by the
vena cava posterior, a new formation first found in dipnoans and
lying, unlike the subintestinal vessel, dorsal to the gut. In the
adult Ascaphus and Bombina, as well as in some adult urodeles,
both postcardinals and the posterior vena cava occur together.
The latter vessel functions alone in dipnoans, which are thus
more advanced in this regard than many Amphibia. The poster-
ior portions of the postcardinals are modified to form a renal
portal system. In Amphibia this system collects blood from the
tail and limbs and sends it to a capillary plexus in the kidneys.
Some of the blood from the hind limbs is returned to the heart
by way of the abdominal veins which are paired vessels associated
with the cardinals in the body wall of sharks, and which represent
the primitive route for returning blood from the hind limbs to
the heart. In Amphibia the abdominal vessels are fused to form
a single conspicuous vessel running along the ventral surface
of the abdominal cavity and emptying, not into the cardinal
veins as in fish, but into the hepatic portal vein. Blood from the
legs must pass, therefore, through either the renal or the hepatic
strainer; it cannot pass directly to the heart without sifting
through a capillary net. The anterior cardinals are less modified
in Amphibia. They receive blood from the internal and external
jugulars as in fish. Dipnoans, with their well-developed lungs,
have anticipated the Amphibia in developing a pulmonary vein
returning blood directly to the heart, but Amphibia have special-
ized for respiration in another direction as well. They have
developed a pair of large veins under the skin of the body to
assist in cutaneous respiration.

The blood vessels leading away from the heart are the arteries.
They differ from most veins in having muscular walls, which
are present, however, in the largest veins. A short distance from
the heart the main vessel, the anterior part of the subintestinal,
divides and sends paired branches to the dorsal side of the gut
by the only route available, namely, by the tissue between the
gill clefts or pouches. The resulting aortic arches may be four
in Amphibia, although two more anterior to these are indicated in
the embryo. In many adult urodeles and all Salientia the fifth

THE CIRCULATORY SYSTEM

187

of these six arches dwindles away. In the Salient) a the third and
sixth arches lose their connection with the dorsal aorta, only the
fourth remaining as the so-called " systemic arch." In the cae-
cilians two aortic arches occur. The arteries leading cranially
from the third arch are the external and internal carotids. The
sixth arch sends a pulmonary artery to the lungs, as well as a
branch to the pharynx. In the lungless salamanders the pul-
monary artery is lost but the arch remains to supply the pharynx
with blood in need of oxygenation. The sixth arch also gives
rise to a cutaneous artery which sends several branches to the
skin where much of the respiration of all Amphibia takes place.
When gills appear during the larval life of most Amphibia, a
direct connection between ventral and dorsal aorta remains at
the base of each gill. With the loss of the gills at metamorphosis
this connecting channel, the original aortic arch, is further devel-
oped. The segmental arteries of the body are decreased in
number in Salientia, apparently in correlation with the modified
metamerism. There are various differences between the blood
vessels of the pelvis of frogs and salamanders. Some of these
are correlated with the loss of the tail in the frog. The arteries
and veins in a typical urodele are shown in Fig. 71 A and B.
Necturus, the species figured, differs from the above description
chiefly in the aortic arches. The sixth, with its pulmonary
artery appears to be part of the fifth which is well developed while
most of the sixth has been lost in the adult in correlation with the
failure of the last branchial cartilage to develop (see p. 102).

Heart. — With the development of lungs in the piscine ancestors
of Amphibia, it became necessary, in order to secure the maximum
efficiency from these organs, to separate those blood channels in
need of oxygen from those already supplied with it by the lungs.
Some dipnoans partly succeeded in accomplishing this necessary
advance by forming an incomplete separation of the two halves
of the single piscine auricle, the left auricle for the blood received
from the lungs and the right for that from the body. The
division of the two blood streams was continued in the ventral
aorta by the formation there of another incomplete partition, the
spiral valve. This same plan of separation is taken over and
further developed in Amphibia with well-developed lungs.

The heart, which may be considered a modified portion of the
subintestinal vessel equipped with striated branching muscle
fibers of a type not found elsewhere in the body, has the form

188

THE BIOLOGY OF THE AMPHIBIA

Fig. 71. — The vascular system of Necturus maculosus. A. Arterial system,
left arm and leg omitted. Ventral aorta and its branches shaded, systemic
arteries in solid line. B. Venous system, viewed ventrally with liver turned to
the right side. Right arm and left leg omitted. (After Miller.) Arterial
system: A.B.I. , first afferent branchial artery; A.B.II., second afferent branchial
artery; A.B.III., third afferent branchial artery; A.O., dorsal aorta; Bs., basilar;
Ca., caudal aorta; C.C., cerebral carotid; Coe.M., coeliaco-mesenteric; Cu.,
cutaneous; E.B.I., first efferent branchial artery; E.B.II., second efferent
branchial artery; E.B.III., third efferent branchial artery; E.C., external carotid;
E.I.M., external inferior maxillary; Epi., epigastric; Fr., femoral; G., gastric; Hp.,
hepatic; I.C., internal carotid; I.I.M., internal inferior maxillary; II., iliac;

THE CIRCULATORY SYSTEM

189

of a tube folded on itself S-fashion. The upper half of the S
is the thin- walled receiving part of the heart; the ventral, the
muscular propelling section. The blood is prevented from flowing
backward by valves, one set placed near the entrance to the heart,
a second between the two main parts, and a third in a double
series in the ventral aorta leading away from it. The receiving
portion of the heart is provided as in fishes with a sinus venosus
which joins the ducts of Cuvier and merges anteriorly into the
atrium. The latter is divided into two auricles completely
separated in frogs and older urodele larvae by a thin septum of
endothelium and connective tissue. The sinus venosus empties
into the right auricle and the pulmonary vein into the left. In
adult urodeles with well-developed lungs a few minute perfora-
tions appear in this membrane, but, as shown by injecting ink
into the living heart, these small holes do not permit an observ-
able mixture of arterial and venous blood (Noble, 1925). The
propelling part of the heart, the ventricle, is not divided by a
septum, but its chamber is crossed by many muscular strands
which tend to hold blood received from the left auricle separate
from that received from the right (Fig. 72). The ventral aorta
or conus arteriosus is furnished with striated muscles and hence
may be considered a part of the heart. Its caudal section or
pylangium is more muscular than the cranial portion or synan-
gium. Two to four semilunar valves that are directed forward
guard the entrance to the pylangium, while the same number of
similar valves are found at its cranial end at the beginning of the
synangium. One of the latter valves in frogs and in most adult
urodeles with well-developed lungs is extended caudally in the
form of a spiral for more or less the entire length of the pylangium.
This valve has important functions in separating arterial from
venous blood as they are forced out from the ventricle.

I.M., inferior mesenteries; K., renal; On., orbito-nasal; Oph., ophthalmic; P., pul-
monary; Sbc, subclavian; Sp., splenic branch of gastric; Sp.', splenic; Sper.,
spermatics; Tr., truncus arteriosus; Vert., vertebral; Vs., vesical. Venous
system: A., anal; Abd., abdominal; C, caudal; Cb., branch of caudal forming
renal portal; Cys., cystic; B.C., duct of Cuvier; F., Fallopian; Fbl., tibial; G.,
branches from stomach to hepatic; H., hepatic; H.P., hepatic portal; H.S.,
hepatic sinus; Hum., humeral; Je., external jugular; Ji., internal jugular; Js.,
jugular sinus; L., lateral; Li., lingual; Mes., mesenteric; N.Or., naso-orbital,
O., ovarian; P., pulmonary; P.C., posterior cardinal; P.Ca., post caval; Pel., pel-
vic; RdL, radial; R.P., renal portal (letters placed just above anastomosis with
posterior cardinal); Sbc, subclavian; Sbm., submaxillary; Sci., femoral; Sp.,
splenic; S.V., sinus venosus; V.Adv., venae advehentes; V.Rev., venae revehentes;
W., ulnar.

190

THE BIOLOGY OF THE AMPHIBIA

The oxygenated blood received from the lungs is squeezed
from the left auricle into the left and caudal part of the ventricle.
The blood that is poor in oxygen is forced from the right auricle
a moment before the blood is sent from the left and tends to
remain on the right side of the ventricle, being held in this posi-
tion by the many muscular strands. Since the conus springs
from this half of the ventricle, this poorly oxygenated blood is
forced out first into the pylangium when the ventricle contracts.

Fig. 72. — Heart of Rana catesbeiana, frontal section, showing the septa which
prevent the mixing of the arterial and venous blood in the ventricle. Ch., chorda;
tendinea; D.A.-V.V., dorsal auriculo-ventricular valve; L.A., left auricle,
L.A.-V.V., left auriculo-ventricular valve; Py., pylangium; R.A., right auricle,
R.A.-V.V., right auriculo-ventricular valve; S.A., auricular septum; Vent.,
ventricle. (After Benninghoff.)

The blood makes its way into the nearest openings and into those
vessels offering the least resistance. These are the openings
into the sixth or pulmonary arches, which because of their
short circuit, are free from the resistance of accumulated blood.
In salamanders the openings to the pulmonary arch lie directly
cephalad of the synangial valves, but in frogs the two pulmonary
arches unite to form a single vessel which opens into the pylan-
gium just caudal of the synangial valves. This position, nearer
the source of supply, is a more favorable one for securing the first
blood passed through the pylangium. As the blood is squirted
into the pylangium, the latter contracts, bringing the free margin

THE CIRCULATORY SYSTEM

191

of the spiral valve against its wall and forcing the blood received
during the latter part of the contraction to flow along only the
ventral surface of the valve and hence to the more ventrally
situated vessels in the synangium (Fig. 73 A). This blood, which
comes from the ventricle last, is the oxygenated blood from the

Fig. 73. — The conus arteriosus of two salamanders opened along the left side
and turned back to show the valves. A. Amby stoma maculatum. B. Plethodon
glutinosus. Sp.V., spiral valve.

left auricle and it is directed into the carotid and systemic arches
by the spiral valve. In Rana, the spiral valve completely shuts
off from the pulmonary arch the systemic flow of blood; but in the
salamanders, where the openings from all the arches lie in the
synangium, it would seem that some mixture must occur. Never-
theless, the directive action of the spiral valve is such that ink
injected into the left auricle is found to be carried only to the
ventral part of the truncus, from the point where the anterior
arches arise.

A further device for making sure that the oxygenated blood be
carried to the head of Amphibia is the development of a so-called
" carotid gland" at the point on the third arch where the internal
and external carotids take origin. This structure is not a gland
at all but merely a spongy enlargement of the arch which offers
further resistance to the blood and steadies the pressure by con-

192

THE BIOLOGY OF THE AMPHIBIA

tinuing to contract between beats. There is also a valvula para-
doxa near this point which may equalize the flow of blood in the
two carotids (Subba Rau, 1924).

Modifications of the Heart. — Many salamanders undergo a
reduction of their lungs, for they live in situations where cutan-
eous and buccopharyngeal respiration alone will suffice. In
these forms the auricular septum becomes greatly fenestrated,
the left auricle reduced, and the spiral and paradox valves lost
(Fig. 73B). A few salamanders with lungs, such as Crypto-
branchus, live in water and do not use them as much as do some
terrestrial forms. In these species the auricular septum is
fenestrated and the spiral valve is lost, while the left auricle still
maintains a large size. The close correlation between the
development of a spiral valve and the functional completeness
of the auricular septum suggests that mechanical factors, such as
the stagnation of blood in the lungs, are responsible during each
ontogeny for the fenestration of the auricular septum. Since
this partition is complete in the late larvae of urodeles, it would
seem that the primitive Amphibia were equipped with hearts
capable of separating arterial and venous streams. Those
modern urodeles, which as permanent larvae continue to live in
the water, or as specialized terrestrial forms have given up the
use of the lungs, exhibit various retrogressive changes in the heart
mechanism. Similar conditions have been described in caecilians.
These Amphibia may be compared to the human fetus which,
unable to use its lungs, maintains a foramen between right and
left auricles, serving to equilibrate the pressures of the two blood
streams.

Although the heart has the form of a twisted tube, it does not
owe this character solely to the pressure of adjacent tissue, such
as the Cuvierian ducts behind and the aortic arches in front. If
the heart rudiment is removed from a frog embryo and cultured
in Ringer's solution, it may grow into a twisted, pulsating organ
(Ekman, 1924) which, however, has not a typical form. Trans-
planting a heart rudiment into the tissues of a second frog embryo
in such a way that it taps the blood supply will give a " parasite"
heart of enormous size while the host's own heart especially the
ventricle, dwindles. Thus function may have an important
effect on the size of the heart or its parts, although only a little
on its general form (Stohr, 1925, 1926). Salamanders of great
length but only moderate girth, such as Siren and Amphiuma,

THE CIRCULATORY SYSTEM

193

Ven

have increased the heart capacity by the development of a series
of pendulent extensions of the auricles (Fig. 74) and the same
maintains in the small, but very slim Pseudobranchus.

Function of the Heart. — The primary function of the heart
is to force blood into the arteries against the pressure caused
by the tonic contraction of the smooth muscle fibers of the arteries
and arterioles. The difficulty is increased by the friction within
these vessels and capillaries as
well as by the viscosity of the
blood due chiefly to the rela-
tive amount of protein held
in colloidal solution in the
blood. The blood pressure
maintained by the heart
must be higher than that of
the osmotic pressure of the
plasma proteins in order to
permit the filtration of urine
through the glomeruli of the
kidney. In the frog the sys-
tolic pressure of the heart is
about three times the osmotic
pressure of the colloids (Bieter
and Scott, 1928).

The output of blood by the
heart must be sufficient to in-
sure an adequate supply of
food and oxygen for the tis-
sues of the body. The blood
flow in the capillaries, because
of their larger total area,

is much slower than in the larger vessels, thus allowing greater
opportunity for gas exchange and other functions of the blood to
take place. The heart output is determined in part, by the stroke
volume of blood but chiefly by the rate of pulsation. The
latter is regulated principally by the vagus which inhibits the
heart rate and by the sympathetic impulses which accelerate it.
Kraupl (1927) has demonstrated the cardio-accelerator effects
upon stimulation of the isolated sympathetic trunk, after cutting
the vagus connection to the heart. The rate is affected by
temperature, gradually increasing with each rise up to a certain

Fig. 74. — Heart of Siren lacertina.
Numerous finger-like processes greatly
increase the volume of the auricles.
L.Au., left auricle; Pyl., pylangium; Syn.,
synangium; Ven., ventricle.

194

THE BIOLOGY OF THE AMPHIBIA

maximum but with a greater increase between 10 to 35°C. than
between lower temperatures (Inukai, 1925). The slowing in
heart rate during cooling is partly compensated for by a reflex
increase in the stroke volume (Schulz, 1906) which tends to
maintain the heart output despite a decrease in heart rate.

Any living tissue after excitation shows a refractory period
during which it is not excitable. This period is much longer in
heart than in skeletal muscle and gives it a rhythmic beat.
Contraction of the heart begins at the sino-auricular node in
Amphibia. It can be shown experimentally that cooling the
zone of union between sinus venosus and right auricle will slow
down the heart rate, while cooling the surface of auricles or ven-
tricles does not have this effect. Although all heart muscles will
contract rhythmically on stimulation, the tissue of the sino-
auricular node is especially sensitive and comparatively rapid in
rate of response. If the heart is removed without the sinus, the
beating is less rapid than when the sinus is left attached to the
isolated heart. Hence the sino-auricular node is the "pace
maker" for the remainder of the heart.

Even though the heart is normally regulated by nervous con-
trol, it can function independent of innervation. Further, each
species seems to have its own rate of pulsation. The heart of
Amby stoma tigrinum transplanted into A. maculatum retained its
own rate in this new environment (Copenhaver, 1927). Weiss
(1927) succeeded in transplanting the hearts of adult Bombina
and noted some effect of the host upon the beat of the trans-
planted heart before a new innervation was established. This
he interpreted as due to a hormone. The recent work of Copen-
haver (1930) indicates that the sinus has not only important
functions in controlling the rate of heart beat in Ambystoma but
may also influence the specific tempo of the beat. The posterior
part of the heart of A. tigrinum may be transplanted into A.
maculatum in such a way that it will combine with the anterior
part of the heart of the latter species. In such cases the posterior
part not only dominates the anterior part by acting as a general
pace maker, but it also imposes its own specific rate upon the
heart parts of the host species.

Blood pressure is increased by a constriction of the arterioles
and capillaries. Stimulation of the medulla of the frog causes a
strong constriction of the arterioles of the webs between the toes
(Bikeles and Zbyszewski, 1918). There are also vasoconstrictors

THE CIRCULATORY SYSTEM

195

in the spinal cord. Besides the nerves, hormones may affect
the constriction of the peripheral vessels. Pituitrin, the hor-
mone of the posterior lobe of the pituitary gland, as well as
adrenalin induces a constriction of the vessels.

Lymphatic System. — Besides the arteries and veins, there is
another system of channels extending throughout the body of
Amphibia. These are the lymphatics, which collect the blood
which seeps through the walls of the capillaries and return it to
the veins. Such blood is devoid of erythrocytes and is, therefore,
colorless, but it contains most of the other ingredients of blood.
It is called " lymph."

The lymphatic vessels may arise by sprouting from embryonic
blood channels in very much the same way as arteries and veins
arise from these plexes, or they may be formed from mesenchyme
independently of preexisting channels (Kampmeier, 1922).
Although the lymphatics closely resemble the bloodvessels in their
origin, they differ in that they frequently widen out to form great
sinuses and make connections with the large pericardial and peri-
toneal cavities. Unlike blood vessels the lymphatics of the intes-
tine absorb fat and are known as "lacteals." The lymph vessels
of urodeles form two main systems: one running parallel to the
aorta and emptying into the subclavian vein of each side, another
lying superficially under the skin and carrying the lymph chiefly to
the postcardinals and cutaneous veins. The lymphatics of the
Salientia are remarkable in forming large sinuses under the skin,
the function of which may be to prevent a rapid drying of the
skin. The lymph in these channels flows towards the heart and
it is pumped into the veins by a series of lymph hearts. In the
caecilians there may be over 200 of these hearts lying flat under
the skin intersegmentally and forcing the lymph into interseg-
mental veins (Marcus, 1908). Each heart, which is a simple sac
of endothelium encircled by a network of striated muscle and a
sheath of connective tissue, receives lymph from several lymph
vessels. Valves prevent the flow of blood from the veins into
the lymphatics. In urodele larvae there may be a series of similar
hearts along the body emptying into the large cutaneous vein.
In tadpoles there is a pair of lymph hearts emptying into the
third intersegmental vein (Fig. 75) and several others along the
tail. Grodzinski (1925) correlates this reduction with the poor
development of the large cutaneous veins in the tadpole. In
adult Salientia there is usually a single pair, the anterior pair

196

THE BIOLOGY OF THE AMPHIBIA

of the tadpole, emptying into the vertebral vein, and a caudal
pair, one on either side of the coccyx, pumping the lymph into a
branch of the ischiadic vein. These hearts may be readily
observed by removing the skin from the end of the coccyx.

Fig. 75. — Reconstruction of the lymphatic vessels of the head of a toad
tadpole showing their relation to the larger blood vessels. Cor.Lym.Ant.Dex.,
right anterior lymph heart; Cor.Lym.Ant.Sin., left anterior lymph heart; Lym.
Jug., lymphatica jugularis; Lym.Lat., lymphatica lateralis; Si.Circ.Or., circumoral
division of sinus maxillaris primigenius; Si. M and., mandibular division; Si.Peri-
card., pericardial division; Si. Temp., temporal division. (After Kampmeier.)

Their beating is independent of that of the heart or of the other
lymph hearts. It is, nevertheless, under nervous control since
cutting away the spinal cord destroys the beat. The lymph
heart tissue is thus neither structurally nor functionally similar to
heart tissue (Briicke and Umrath, 1930). The number of
lymph hearts varies with the species. In the primitive Ascaphus

THE CIRCULATORY SYSTEM

197

there may be three pairs of lymph hearts near the coccyx, and
some brevicipitids and pipids may have two or three pairs. Even
Rana, which is usually described as having only one pair of poste-
rior lymph hearts, may have this one divided into three pairs
(Jolly and Lieure, 1929).

The amount of lymph flowing through the four small lymph
hearts of frogs is very remarkable. Isyama (1924) estimated
that the entire blood plasma goes through these portals fifty
times a day. This speed of lymph circulation, much greater than
in mammals, is a consequence of the greater permeability of the
blood vessels in Amphibia (Conklin, 1930). It demands, more-
over, a mechanism of the rapid return of the lymph to the blood
vessels in order that the blood volume be not seriously lowered.
The lymph heart system of Amphibia is well developed as an adap-
tation to meet the exigencies of a rapid turnover of lymph. If the
hearts become clogged or otherwise fail, the frog soon becomes
edematous and dies because of the isolation of valuable con-
stituents of the blood in the lymph spaces.

The lymphatics may have special functions to perform. At
times of injury those near the wound gather up extravasated
erythrocytes lying near the lymphatic capillaries. The eryth-
rocytes seem to exert a specific attraction on the endothelium of the
lymphatic capillaries which send out sprouts for a distance as
great as 76 microns and gather up the red blood cells, finally
to return them to the veins intact (Clark and Clark, 1925). If
the erythrocytes are further away than this distance, or remain
there over 12 hours, the wandering macrophages phagocytose
them.

References

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Beyer, W., 1921: tTber kernlose rote Blutkorperchen bei Amphibien,

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THE BIOLOGY OF THE AMPHIBIA

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, 1930: Results of heteroplastic transplantation of anterior and pos-
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throplastids in vertebrates other than mammals, Amer. Jour. Anat.,
XXX, 347-405.

, 1925: Studies on the non-nucleated cytoplasmic elements of the

blood. 3. Leucoplastids or non-nucleated leucocytic derivatives in
vertebrates other than mammals, Amer. Jour. Anat., XXXV, 31-62.

Federici, E., 1926: Recherches experimentales sur les potentialites de
l'ilot sanguin chez l'embryon de Rana fusca, Arch. Biol., XXXVI,
465-487.

Frase, W., 1930: Zellengrosse als Leistungsfaktor der Haustiere, Der Natur-

forscher, VII. 221-224.
Goss, Charles M., 1928: Experimental removal of the blood island of

Amblystoma punctatum embryo, Jour. Exp. Zool., LII, 45-64.
Grodzinski, Z., 1924: tiber die Entwicklung der Gefasse des Dotterdarmes

bei Urodelen, Bull. Int. Acad. Polon. Sci. Let. Cracovie, Ser. B, 1924,

57-67, 1 pi.

, 1925: Weitere Untersuchungen iiber die Blutgefassentwicklung bei

Urodelen, Bull. Int. Acad. Polon. Sci. Let. Cracovie, Ser. B., 1925,
195-209, 1 pi.

Heesen, Wilhelm, 1924: tiber die Zahlenverhaltnisse der roten und
weissen Blutkorper der heimischen Amphibien im Wechsel der Jahres-
zeiten, Zeitschr. vergl. Physiol., I, 500-516.

THE CIRCULATORY SYSTEM

199

Hilton, W. A., 1913: The development of the blood and the transformation
of some of the early vitelline vessels in Amphibia, Jour. Morph., XXIV,
339-382.

Inukai, T., 1925: tiber den Einfluss der Temperatur auf die Pulsationzahl
bei den Amphibienlarven und Vogelembryonen, Japan Jour. Zool,
I, 67-75.

Isayama, Sunao, 1924: tiber die Geschwindigkeit des Fliissigkeitsaustausches
zwischen Blut und Gewebe, Zeitschr. Biol, LXXXII, 101-106.

Jolly, J., and Lieure, C, 1929: Sur les coeurs lymphatiques des Anoures,
Compt. rend. Soc. Biol. Paris., CI, 1063-1066.

Jordan, H. E., and C. C. Speidel, 1923: Blood cell formation and destruc-
tion in relation to the mechanism of thyroid accelerated metamorphoses
in the larval frog, Jour. Exp. Med., XXXVIII, 529-541.

, 1923a: Studies on lymphocytes; I. Effects of splenectomy, experi-
mental hemorrhage and a hemolytic toxin in the frog, Amer. Jour.
Anal, XXXII, 155-188, 5 pi.

, 1924: Studies on lymphocytes; III. Granulocytopoieses in the

salamander with special reference to the monophyletic theory of blood
cell origin, Amer. Jour. Anal, XXXIII, 483-505, 2 pis.

, 1925: Studies on lymphocytes; IV. Further observations upon the

hemopoietic effects of splenectomy in frogs, Jour. Morph., XL, 461-477.

Kampmeier, O. F., 1922: The development of the anterior lymphatics and
lymph hearts in anuran embryos, Amer. Jour. Anal, XXX, 61-131.

Kingsbury, B. F., 1912: Amphibian tonsils, Anal Anz., XLII, 593-612.

Kraupl, F., 1927: tiber reine Reizung der Forderungsnerven am Frosch-
herzen, Arch. ges. Physiol, CCXVII, 327-342.

Marcus, H., 1908: Beitrage zur Kenntnis der Gymnophionen ; II. tiber
intersegmentale Lymphherzen nebst Bemerkungen uber das Lymph-
system, Morph. Jahrb., XXXVIII, 590-607, 1 pi.

Maximow, A., 1910: tiber embryonale Entwickelung der Blutzellen bei
Selachiern und Amphibien, Anal Anz. Erghefl, XXXVII, 64-70.

Moore, Julia S., 1915: The growth of the vascular system as it is correlated
with the development of function in the embryos of Amblystoma,
Anal Rec., IX, 109-111.

Myers, M. A., 1928: A study of the tonsillar developments in the lingual
region of anurans, Jour. Morph. Physiol, XLV, 399-433.

Noble, G. K., 1925: The integumentary, pulmonary, and cardiac modifica-
tions correlated with increased cutaneous respiration in the Amphibia:
A solution of the "hairy frog" problem, Jour. Morph. Physiol., XL,
341-416.

Pentimalli, F., 1909: tiber die Zahlverhaltnisse der weissen Blutkorperchen
bei den Amphibien in verschiedenen Zustanden, Int. Monatsschr. Anal
Physiol, XXVI, 206-222.

Ponder, Eric, 1924: The erythrocyte and the action of simple haemoly-
sins, Biol. Monog. and Manuals, II, Edinburgh.

Schulz, N., 1906: Studien uber das Verhalten des Blutdruckes von Rana
esculenta unter den verschiedenen ausseren Bedingimgen, insbesondere
bei verschiedener Korpertemperatur, Arch. ges. Physiol, CXV, 386-445,
6 pi.

200

THE BIOLOGY OF THE AMPHIBIA

Smith, H. M., 1925: Cell size and metabolic activity in Amphibia, Biol.

Bull, XLVIII, 347-378.
Stohr, P., Jr., 1925: Zur Entstehung der Herzform, Anat. Anz. ErghefL,

LX, 105-112.

, 1926: Zwei neue experimentelle Resultate zur Herzentwicklung bei

Amphibien, Anat. Anz. ErghefL, LXI, 151-153.
Subba Rau, A., 1924: Observations on the anatomy of the heart, lungs and

related parts of Ceratophrys, Jour. Anat. London, LVIII, 306-327.
Weiss, P., 1927: Herztransplantation an erwachsenen Amphibien, Arch.

ges. Physiol, CCXVII, 299-307.

CHAPTER IX

THE DIGESTIVE SYSTEM

Life on land necessitated a profound change in the anterior
portion of the digestive tract. A tongue for the seizing and
swallowing of food developed to meet the new conditions of life.
As shown in the ontogeny, this structure was formed by the
addition of a glandular fold anterior and lateral to the piscine
tongue rudiment. Fishes lack multicellular glands in the mouth,
but the first tetrapods, to judge from the fenestrae in the palates
of labyrinthodonts, were equipped with a glandular mass behind
the premaxillaries. In Salientia and Caudata this gland opens
by one or more ducts in the roof of the mouth. Many Salientia

Fig. 76. — Two types of tongue form in plethodontid salamanders. In
Desmognathus fuscus (A) the tongue is attached in front, while in Eurycea
bislineata (B) it is free all round and capable of projection well beyond the
mouth.

have, in addition, a glandular mass in the palatine region (Cohn,
1910). It is apparently this mass which has extended in Brevi-
ceps to cover the greater part of the roof of the mouth. The
chief function of all these glands would seem to be to render the
tongue more adhesive. Most Salientia have the tongue attached
by resistent tissue to the front angle of the jaws and capable of
projection only by flapping the posterior part over and beyond
the anterior. A few frogs in different parts of the world have
succeeded in freeing the anterior attachment, and many of the
common urodeles have the tongue in the shape of a mushroom,
capable of projection several times the length of the head (Fig.

201

202

THE BIOLOGY OF THE AMPHIBIA

76). It is remarkable that this boletoid tongue is found in such
moderately aquatic types as the Red Salamander (Pseudotriton)
and yet is lacking in the terrestrial Plethodon. Thoroughly
aquatic Salientia tend to reduce the tongue, and both this structure
and the intermaxillary gland are lacking in the Pipidae.

The lining of the mouth differs from skin chiefly in possessing
numerous mucous or goblet cells and in lacking subepithelial
mucous glands and pigment. Taste buds are present on tongue
and palate. Cilia are present on these regions in terrestrial
Amphibia but are lacking in larvae and in throughly aquatic
types such as Leurognathus. They are especially active in the
vicinity of the intermaxillary gland outlets. Unlike the cilia
covering the body of the embryo, they appear to be under
sympathetic control (McDonald, Leisure, and Lenneman, 1928).

The oesophagus is frequently separated from the mouth cavity
by a fold. Its lining is thrown into a number of more or less
persistent longitudinal folds and is ciliated. The presence of
cilia suggests that the peristaltic action of the oesophageal
muscles is not adequate to keep the food moving along by their
efforts alone as in the case of higher vertebrates. The epithelium
of the oesophagus agrees with that of the mouth in histological
structure. Goblet cells are numerous. In some brevicipitids
the dorsal folds of the oesophagus are composed largely of these
goblet cells which are massed to form a mucus secreting pad.
Oesophageal glands are found just before the stomach of Rana
and Bufo but do not occur in various more primitive Salientia
or in certain urodeles (Kingsbury, 1894). They are pepsin-
secreting structures and may be considered modified stomach
glands (Bensley, 1900).

Stomach. — The stomach is not sharply marked off from the
oesophagus. Both are provided with an outer longitudinal and
an inner circular layer of smooth muscles. Within this muscularis
and separated from it by a well-vascularized layer of connective
tissue is another outer sheath of longitudinal muscle fibers and an
inner, of circular fibers. These form the muscularis mucosae, a
thin layer of muscle lying directly adjacent to the glandular
lining of the stomach. The muscles function in passing the food
posteriorly and in mixing it with gastric juice in the stomach.
If disagreeable substances are swallowed, a frog is able to reverse
this action and turn the stomach inside out, until it bulges far
outside the mouth. The stomach usually lies to the left of the

THE DIGESTIVE SYSTEM

203

midline and is curved with the convex side toward the left,
held in place by two folds of the
peritoneum (Fig. 77). Its lining or
mucosa consists of a simple, colum-
nar epithelium on which there
empty great numbers of small glands.
Those at the oesophageal end of the
stomach consist of a long neck of
the same structure as the surface
epithelium, a few large and trans-
parent mucous cells, and one or more
diverticula of cells having a granular
cyptoplasm (Fig. 78). The latter
cells apparently secrete both pepsin-
producing granules and hydro-
chloric acid. In mammals two
different types of cells perform
these functions. The glands near
the pylorus are comparable to
the necks of the other glands.
Large mucous cells are occasion-
ally found at the bottom of the
pyloric glands giving further
evidence of this homology. The
stomach of Amphibia serves to
alter both physically and chemically
the food swallowed; it functions
also as a place of food storage.
Food may be available only at
irregular intervals and many frogs
are able to expand their stomachs
enormously when filling them on
these occasions.

Intestines. — The intestine in
Amphibia is a tube of

It is

Fig. 77. — Viscera of Necturus
maculosus. Cl.G., cloacal
glands; D.M., dorsal mesentery;
H., heart; Int., intestine; K.,
nearly kidney; Li., liver; Lu., lung;

uniform width except posteriorly ^S^f^— ,
where it widens to form the large T., testis; U.B., urinary biad-

• i j • t, . 1 , . l , der; W.D., Wolffian duct.

intestine. It is nearly straight (Modified from Cope.)
in some caecilians and only slightly

folded in Siren and Proteus. Increase in length reaches its
extreme stage in the common Rana tadpoles, where the small

204

THE BIOLOGY OF THE AMPHIBIA

intestine is coiled in watch-spring fashion. The intestine
possesses the same longitudinal and circular muscle layers as the
stomach. Its mucosa consists of columnar and goblet cells, the
former having absorptive functions. The mucosa is thrown into
many longitudinal and transverse folds which like the villi of the

M. B.

LMu. C.

fS.C. s.c

C.T._2

Gl. CU

Sec. C.

Fig. 78. — Stomach glands of a salamander. A. Two gastric tubules from the
middle region of the stomach of Necturus maculosus. B. Section through a
pyloric-gland tubule. C.T., connective tissue; Gl.C, gland cells; M.B., muci-
genous border of surface cells; Mu.C, mucous cells; N., neck of the gland; S.C,
surface cells of the stomach; Sec.C, secreting cells of the fundus of the gland.
(After Kingsbury.)

mammalian intestine afford a greater absorptive surface. The
cross-folds delay the passage of food, and Jacobshagen (1915)
believes their arrangement may have some systematic value.
Urodeles but no frogs have glands between the folds of the small
intestine. They resemble the pyloric glands of the stomach,
although ducts may be absent (Goldsmith and Beams, 1929).
The small intestine is sharply marked off from the stomach by

THE DIGESTIVE SYSTEM

205

the pyloric constriction. In higher Salientia it is equally well
demarcated from the large intestine by a valve or ring fold.
The large intestine usually presents a differentiation into two
parts, an anterior larger reservoir for feces and a posterior more
muscular part. A slight asymmetrical enlargement of this ante-
rior section has been considered in some frogs and urodeles to
represent a rudimentary caecum (Crofts, 1925). It is covered
with lymphoidal tissue.

Glandular Outgrowths. — Associated with the anterior part of
the small intestine are the liver and the pancreas, the two glan-
dular outgrowths of the embryonic midgut common to all verte-
brates. The liver develops very early in Rana by the formation
of a cavity in the vitelline mass. A diverticulum is produced
from the antero-ventral margin of the cavity (Weber, 1903) and
develops into a compound tubular gland. The cavity and proxi-
mal portion of the gland are transformed into a hepatic duct.
A gall bladder is formed as a reservoir for the secretion of the
gland. The pancreas arises near the liver in the form of three
outgrowths from the intestinal wall, which soon fuse to form a
single structure. The distal portions of the outgrowths form
glands of the tubular or acinous type; the proximal portion, the
ducts. In urodeles two of the ducts empty into the intestine,
the anterior behind the pylorus and a posterior in association
with the hepatic duct. In Salientia the more anterior duct
is lost (Goppert, 1891). Of especial interest are a series of cell
aggregations between the tubular glands of the pancreas; these
are the islets of Langerhans. They develop without ducts and
produce a secretion which is passed directly into the blood stream.
Intestine, liver, and pancreas are covered with peritoneum which
lines the body cavity and forms the mesenteries which hold the
organs in place.

Digestion. — Food is needed for growth and repair, also for
energy to perform the daily round of activities. The simple
chemical elements cannot be used for food. They must be first
combined into molecules often of extreme complexity. The
compounds — proteins, carbohydrates, and fats — constitute foods.
Certain salts, water, and apparently vitamines are also indis-
pensable. Adult Amphibia live largely on insects or other
invertebrate prey and hence their food is rich in proteins. These
perform the definite function of renewing the worn-out tissues of
the animal and when digested may be resynthesized to form

206

THE BIOLOGY OF THE AMPHIBIA

carbohydrates. The latter are stored in the organism mainly
in the form of the insoluble substance glycogen. The glycogen,
when needed, is converted into some form of sugar (mostly glu-
cose) which on oxidation is the greatest source of energy in all
animals. Starvation in Amphibia as well as in man quickly
leads to the depletion of the carbohydrate stores. Hence the
energy for the fasts, which are perhaps not rare in Amphibia,
must be furnished by the fat reserve or by the tissue protein.
Since fat is stored in practically a pure form, while protein is not,
the storage of energy in the form of fat is much more economical
than in the form of protein. Nevertheless, Amphibia are lean
animals and never have learned the trick of developing the great
stores of fatty tissue seen in birds and mammals. Perhaps
cold-blooded animals, with their low metabolism, have no need
of these stores of potential energy, or perhaps one of the reasons
for their never becoming warm-blooded is the leanness of their
bodies.

Digestion in Amphibia follows, on the whole, the typical
vertebrate pattern known to us in our own bodies, however, with
certain modifications. An insect seized by a frog is quickly
swallowed, the small teeth crushing it only to a small extent and
the secretions of the mouth serving merely as a lubricant.
Digestion first begins in the stomach where the gastric glands
secrete hydrochloric acid and also an enzyme, pepsin, which
acts solely on the proteins transforming them into substances
of smaller molecular weight. A second enzyme, rennin, has been
shown by Kingsbury (1894) to be present in the stomach of
Necturus, but as no Amphibian normally drinks milk on which
this enzyme is well known to act in mammals, its function in
Amphibia is obscure.

The partly digested food rendered acid by the gastric juice is
passed on to the intestine. The intestinal glands activated by
this acid produce a substance secretin, which is released not into
the intestine but into the blood. On reaching the pancreas,
secretin causes the pancreas to pour forth its highly alkaline
secretion which stops the action of pepsin but initiates a second
series of digestive processes. This pancreatic juice contains
three additional enzymes. The most important for the carniv-
orous diet of Amphibia is trypsin which is secreted in an inactive
form, trypsinogen, but is rendered active by a substance secreted
by the intestinal wall. It continues the protein digestion begun

THE DIGESTIVE SYSTEM

207

in the stomach and carries it well on toward the final products
of this digestion chiefly to the peptone stage. The other two
enzymes are an amylase, which changes starches into sugars,
and a lipase, which causes a splitting of the fats into fatty acid
and glycerol. The liver secretes bile, which renders the fats
more readily attacked by the lipase. Finally, the intestinal
juice produced by the mucosa of the intestinal walls contains
enzymes which complete the process of digestion. Of these
the most important is erepsin which acts on the peptones and
thus completes the work begun by the pepsin and trypsin of
liberating the amino-acids from the proteins.

The secretion of the liver contains no digestive enzymes. The
liver, which occupies such a large part of the body cavity, is
not primarily an organ of digestion. It is concerned chiefly in
the further elaboration of the fatty substances, in the storage of
glycogen, in the formation of urea, and finally in the destruction
of the red blood corpuscles. The importance of the liver as a
place of fat storage in cold-blooded forms is particularly empha-
sized during hibernation and in the early spring mating season,
(Buddenbrock, 1928; Berg, 1924), since fat can be most rapidly
mobilized from this organ. By determining the ratio of carbon
dioxide produced to the oxygen utilized during respiration, it is
possible to analyze the nature of the oxidation processes occurring
at any one time. If this respiratory quotient — the volume
of carbon dioxide given off divided by the volume of oxygen
absorbed — is higher than 0.80, carbohydrate is being oxydized in
excess of protein and fat, while a quotient less than 0.80 indicates
that fat oxidation predominates. Dolk and Postma (1927) by
the use of this method have demonstrated that the hibernating
frog uses its fat and not its glycogen reserves.

Absorption and Assimilation. — The products of digestion are
absorbed by the walls of the intestine. The amino-acids are
gathered up by the mesenteric veins and transported to those por-
tions of the body where they are needed for building up the
tissues. Here they are reconverted into the proteins. Those
amino-acids which are not required for building are broken
down by the liver. The nitrogenous part is excreted as urea
while the remainder is formed into carbohydrates which supply
energy to the organism. The amino-acids and sugars are passed
by the intestinal epithelium into the capillaries, while the prod-
ucts of fat digestion seem to be usually transmitted to the lymph

208

THE BIOLOGY OF THE AMPHIBIA

vessels. The sugars that are not used as an immediate source
of energy are stored in the form of glycogen or animal starch.
Proteins cannot be stored as such, but after they are deaminized
the remainder may be converted into glycogen. Various tissues,
especially the muscles, store glycogen, but the liver serves as the
general depot. The latter releases carbohydrates to the blood
in the form of glucose as it is required. In the fall, before
hibernation, the liver of some frogs may be more than twice as
large as in early summer, due chiefly to the increased storage of
glycogen. The fats, not used at once by the tissues, are stored
chiefly in the liver and the adipose body, the latter being a modi-
fication of the genital tract found just anterior to the gonads.
Some frogs have a conspicuous fat body just anterior to the
clavicles, and various narrow-mouthed toads have small, fat
bodies under the skin. In salamanders large accumulations of
fat are usually to be found in the tail. In Proteus, fatty tissue
forms a thin sheet under the skin (Maurer, 1911). By means
of vital dyes, Hadjioloff located a number of small deposits of
fat about the heart and in the pelvic region of various European
frogs. Apparently it is an accumulation of fat which gives the
greenish color to the bones of some of the more translucent
species of tree frog, for Hadjioloff found considerable fat in the
bone marrow of the frogs he studied.

The more indigestible food is retained for a time in the large
intestine which is enlarged anteriorly. Such an enlargement of
the intestinal tract first makes its appearance in Amphibia. It
would seem to serve not only as the last region of food absorption
in the gut but also as a storage place for the feces. At intervals
the excreta are passed out through the cloacal orifice to the
outside.

The waste products of growth and repair of the tissues are
released into the blood stream in the form of urea, carbon dioxide,
water, and various soluble products of protein metabolism. The
carbon dioxide is eliminated from the body by the organs of
respiration. The other waste products are collected from the
blood by the kidneys. The liver also serves as an organ of
elimination of nitrogenous waste products. These are passed
with the bile into the intestine and are excreted with the feces.

Modifications of Digestive Tract. — The absorbing surface of
the digestive tract is increased in Amphibia not by the formation
of pyloric caeca or spiral valves, as in fish, but merely by an increase

THE DIGESTIVE SYSTEM

209

in length. Great length without great bulk is secured by the
narrowing of the tube and its twisting into a compact spiral.
Most frog tadpoles feed largely on water plants and like other
vegetarians require a maximum amount of absorbing surface.
The winding of the intestine is not in one plane but extends
ventrally as the spiral becomes narrower. There are usually two
and a half to three loops, but as each loop is double, the winding
seems more extensive. A few tadpoles living in the confined
space between the leaves of bromeliads or banana plants feed to
a considerable extent on frog eggs. Their intestines do not have
the characteristic watch-spring form of most tadpoles but are
short and resemble the intestines of the adult frog in lacking a
spiral. The more carnivorous tadpoles, such as those of Cera-
tophrys dorsata, have a shorter digestive tract than herbivorous
forms.

It is probable that many of these differences in length and form
of the intestines of tadpoles is due to the character of the food
during each ontogeny (Fig. 79). In view of the experiments of

Fig. 79. — Effect of food on the intestine of tadpoles. A. Intestine of a tadpole
reared on a plant diet. B. Intestine of another reared on an animal diet. {After
Babak.)

Yung (1904, 1905), the mechanical effect of bulky food would
seem to be greater than the chemical effect of plant tissues on
the digestive tract of the tadpole. The experiments of Babak
(1905, 1911) suggest that the chemical factor may also play a
part in controlling the length of the digestive tract.

The environment affects the digestive processes of Amphibia
directly. M tiller (1922) has shown that the digestive action of
the frog pepsin increases with rising temperature reaching an
optimum at 40°C, a temperature at which few frogs will survive.
Thus the optimum conditions for digestion are not the best
temperatures for the health of the frogs.

Amphibia are able to withstand long fasts. Tadpoles may live
for months without food. This would seem to be due to their
ability to feed on bacteria or other small particles in the water

210

THE BIOLOGY OF THE AMPHIBIA

(Bock, 1925; Krizenecky and Petrov, 1926). Nevertheless,
some urodeles such as Proteus, which are not known to have this
ability, have been kept for over a year without food. Axolotls
have been reported to live 650 days without food (St. Hiller,
1929). During this time they lost 81 per cent of their initial
weight. Although Amphibia with their low metabolic rate
might be expected to withstand longer fasts than warm-blooded
animals, their ability to live for months on their own tissues is
remarkable for active vertebrates.

References

Babak, E., 1905: tiber die morphogenetische Reaktion des Darmkanals der

Froschlarve auf Muskelproteine verschiedener Tierklassen, Beitr.

Chem. Physiol, VII, 323-330.
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enen und artfremden Proteinen Zentralbl. Physiol., XXV, 437-441.
Bensley, R. R., 1900: The oesophageal glands of Urodela, Biol. Bull,

II, 87-104.

Berg, W., 1924: tiber funktionelle Leberzellstrukturen; III, Periodische
Veranderungen im Fettgehalt der Leberzellen des im Winter hungernden
Salamanders und ihre Ursachen, Zeitschr. Mikr. Anat. Forsch., I,
245-296, 2 pis.

Bock, Friedrich, 1925: Weiterer Beitrag zur Frage der Ernahrung von
Amphibienlarven durch im Wasser Geloste Nahrstoffe, Zool. Anz.,
LXIV, 261-276.

Buddenbrock, W. von, 1928: "Grundriss der vergleichenden Physiologic,"
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Cohn, L., 1910: Zur Kenntnis der Munddrusen einiger Anuren, Zool. Jahrb.
Suppl, XII, 719-724.

Crofts, Doris R., 1925: The comparative morphology of the caecal gland
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thyopsida and Sauropsida, Proc. Zool. Soc. London, 1925, 101-188.

Goldsmith, J. B., and H. W. Beams, 1929: A study of the intestinal glands
of some urodeles, Trans. Amer. Micr. Soc, XL VIII, 292-301, 2 pis.

Goppert, E., 1891 : Die Entwicklung und das spatere Verhalten des Pancreas
der Amphibien, Morph. Jahrb., XVII, 100-122, 1 pi.

Hadjiolopf, A., 1930: Recherches sur le tissue adipeux chez les poissons et
la grenouille, Bull Hist. appl. physiol. path. tech. micros., VII, 8-20.

Jacobshagen, E., 1915: Zur Morphologie des Oberflachenreliefs der
Rumpfdarmschleimhaut der Amphibien, Jena. Zeitschr., LIII, 663-716.

Kingsbury, B. F., 1894: The histological structure of the enteron of Necturus
maculatus, Proc. Amer. Micr. Soc, XVI, 19-65.

Krizenecky, J., and I. Petrov, 1926: Weitere Untersuchungen uber das
Wachstum beim absoluten Hungern, Arch. Entw. Mech., CVII, 299-313.

McDonald, J. F., C. E. Leisure, and E. E. Lenneman, 1928: Newly dis-
covered controls of ciliary activity, Amer. Jour. Physiol, LXXXV, 395.

THE DIGESTIVE SYSTEM

211

Maurer, F., 1911: Die ventrale Rumpfmuskulatur von Menobranchus,

Menopoma und Amphiuma, verglichen mit den gleichen Muskeln

anderer Urodelen, Jena. Zeitschr., XLVII, 1-40.
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Frosches und der Warmbluter? Arch. Ges. Physiol, CXCII, 214-224.
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Bull. Int. Acad. Polon. Sci. Let, 1928, 191-216.
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les vertebres, Arch. Anat. Micr., V, 487-727, pis. 17-27.
Yung, E., 1904: De Tinfluence du regime alimentaire sur la longueur de

l'intestin chez les larves de Rana esculenta, Compt. rend. Acad. Sci.

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Experiences sur les larves de Rana esculenta, Compt. rend. 6me Congr.

int. Zool. Berne, 297-314.

CHAPTER X

THE SKELETON

In a preceding chapter we have traced the emergence of the
first tetrapods from their fish ancestors and have seen that after
vertebrate life became established on land it reverted not once
but many times to the aquatic habitat and that this occurred
frequently long before the first modern Amphibia appeared.
The skeleton of the early Amphibia shows reductions and other
specializations for which there cannot always be found a close
environmental correlation. In other words, the skeleton might
be considered as something quite independent of the environment
changing progressively because of inherent capacities or restric-
tions. Certain trends of evolution became established and were
apparently automatically carried through to an extreme special-
ization. The same phenomenon is seen to a lesser extent among
modern Amphibia, for the families of Salientia may have arboreal,
aquatic, or fossorial members with the family characters well
defined. It is, therefore, important to isolate as far as possible
the slow, progressive changes from the more rapid and adaptive
ones. This may be accomplished best by describing the pro-
gressive changes in the skeletal elements or, in other words, by
reviewing briefly the history of the various parts of the skeleton.

Skull. — The skull of the first tetrapods resembled closely that
of their fish ancestors and differed from that of modern Amphibia
in the greater number of skull elements, in the greater extent of
ossification of the chondocranium or cartilaginous brain case, and
in its shape, the early tetrapod skull being high as in most fishes
and in all Sauropsida instead of flattened as in modern Amphibia.
A thick interorbital septum was present, and the brain lay above
the septum.

The skull of the Embolomeri agreed closely with that of the
osteolepid fishes. The number and arrangement of the elements
forming the skull roof were very similar. In both fish and
Amphibia the lateral-line canals were present and crossed the
same bones: namely, the lacrimal, prefrontal, jugal, postorbital,

212

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213

postfrontal, supra, and intertemporals. The spiracle had,
apparently, become replaced by a tympanum, for the spiracular
notch of Osteolepis had the same relation to the skull bones as
the otic notch of the Embolomeri (Watson, 1926). The palate
of fish and Amphibia agreed in most details. The interpterygoid
vacuities were small, and large labyrinthodont teeth were present
in both fish and tetrapods. Since internal nares were present
in the osteolepids, the latter apparently breathed in the manner
of Amphibia. The lower jaw of the Embolomeri was identical
with that of the Osteolepidae and differed strikingly from that
of modern Amphibia in the large number of bones of which it was
composed. It was sheathed outwardly by the dentary and
surangular, mesially by three coronoids and a prearticular,
ventrally by two splenials and the angular. Only dentary and
one other element are invariably present in modern forms,
as will be seen below. The dentary and coronoids carried large
teeth which were replaced alternately like those in the upper jaw.
A shagreening of small teeth was present on the coronoids and
prearticulars of some forms.

The chief difference between the skulls of osteolepids and of
Embolomeri was to be found in the brain case. The basioccipital
condyles of both were single, and the basisphenoids had basiptery-
goid processes with which the epipterygoids articulated. Poste-
rior to this basisphenoid, as shown in Fig. 2, a large part of the
floor of the brain case, or basis cranii, of the osteolepids remained
unossified. Although the osteolepids may not have been the
immediate ancestors of the tetrapods, the resemblance in skull
roof, jaws, and palates are so close that we may consider them as
having the ancestral type of fish skull from which the amphibian
skull was derived.

Progressive Modification of the Skull. — With the origin of the
Embolomeri, the highly complex skull inherited from the fishes
began to undergo a progressive fenestration. The bones appar-
ently tended to segregate along lines of greatest stress. A second
change was the apparent shortening of the skull, for while the
Embolomeri retained 12 cranial nerves, the more advanced
labyrinthodonts show a gradual shifting posteriorly of the hypo-
glossal fenestra until in the stereospondyls the hypoglossal nerves
lay posterior to the skull as in the case of modern Amphibia.
Most reptiles and all mammals have retained the primitive num-
ber of 12 cranial nerves within the skull. It is clear, therefore,

214

THE BIOLOGY OF THE AMPHIBIA

that the heads of modern Amphibia differ from those of the first
tetrapods and of the higher modern forms in that they contain
three fewer somites. This loss has been largely in the occipital
or " vertebral" part of the skull. Just as any of the posterior
vertebrae of a frog are apparently able to produce sacral dia-
pophyses when properly stimulated by the presence of the ilium,
so any one of these three or four skull vertebrae is apparently
able to produce exoccipitals or basioccipitals if the head size
demands it. The homology of the occipital elements lies not
so much in their somites of origin as in their mutual relationship
and their phylogenetic origin.

Another fundamental change in the evolution of the skull
within the labyrinthodonts was its gradual flattening, the tra-
beculae of the higher types being no longer squeezed together.
As a result, the forebrain was dropped lower and lower in the brain
case until finally it came to rest on the dorsal surface of the
parasphenoid. This progressive flattening reached its extreme in
certain stereospondyls and in the aquatic Salientia and Caudata,
although all along the line aquatic forms were frequently more
flattened than terrestrial ones.

In the evolution of the Labyrinthodontia, and to a certain
extent of the other orders of Amphibia, there was a progressive
weakening of ossification. Basioccipital, basisphenoid, and
supraoccipital became reduced in the Labyrinthodontia and have
disappeared entirely in the modern Amphibia. Stadtmiiller
(1929) has described a separate ossification in the brain case of
Triturus alpestris, however, which he interprets as a basioccipital.
In this way, the original single condyle of the fishes was progres-
sively modified into a tripartite and later into a bipartite condylar
surface. Withdrawal of the basioccipital in the reptile series leads
to exactly the same result, in the promammals to the production
of a pair of widely separated condyles like those of modern
Amphibia. This is a striking example of convergence, that is, of
similar changes in unrelated forms.

Accompanying these major changes, there were a number of
minor ones, some destined to produce characteristic structures
in the modern forms. The pineal foramen which occurred
between the frontals of the osteolepids shifted back to between
the parietalsin the first tetrapods and finally disappeared entirely.
In the reptiles it was retained even to recent times in some forms.
The loss of elements in the skull roof was closely correlated with

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215

an increase in the size of the eye, and the reduction of the ele-
ments in the temporal region gave greater freedom to the tem-
poral muscles. Thus, the solid domelike skull roof of the
Embolomeri was restricted enormously during evolution until
in the frogs only the premaxillary, maxillary, septomaxillary,
nasal, quadratojugal, squamosal, frontal, and parietal bones are
left. The urodeles are more primitive than the frogs in retaining
in some species both lacrimals and prefrontals in addition to these
other elements. Further, the frontals and parietals of each side
are free from one another, not fused as in frogs. In some frogs,
such as Xenopus, the fronto-parietals of each side may be more
or less fused posteriorly with one another. The quadratojugal
appears as a separate element in the urodeles only during
ontogeny. Probably temporal muscles were largely responsible
for the cleaning off of surface bones from the temporal region
of the skull of modern Amphibia. In some urodeles the temporal
muscles extend beyond the skull and attach to the cervical verte-
brae.

The cartilage bones of the brain case, as stated above, also
undergo both degeneration and loss during the phylogeny of the
Amphibia. The anterior wall of the ear capsule ossifies as a
prootic in most frogs and some salamanders, while a separate
center of ossification, the opisthotic, appears in the posterior
wall of this capsule in Ambystoma, Necturus, Siren, and a few
other urodeles. The ossification from the prootic extends
posteriorly, while that of the exoccipital spreads into the posterior
wall of the ear capsule in most Amphibia. In higher urodeles
and in frogs a separate opisthotic never appears, while in the
Plethodontidae neither prootic, opisthotic, nor exoccipitals form
separate ossifications even in the larvae. This is a specialization
away from the labyrinthodont condition. The exoccipitals and
prootics frequently fuse in Salientia and in some pipids the
combined bones of the two sides may fuse to form a single
element. In most Salientia and Caudata the interorbital walls
of the brain case ossify to form a sphenethmoid on each side.
In some species, especially in burrowing types, the ethmoid may
also ossify and fuse with the sphenethmoid. Slow-moving
aquatic Amphibia have their brain cases least ossified ; burrowing
types have them usually the most ossified.

Modification of the Palate. — Progressive changes in the palate
region went forward even more rapidly than those on the roof

216 THE BIOLOGY OF THE AMPHIBIA

of the skull or in the brain case. Most conspicuous of these
changes was the increase in size of the interpterygoid vacuities
and the corresponding reduction in width of the pterygoids.
The pterygoids within the Labyrinthodontia lost their connection
with the basipterygoid processes and in the advanced types were
supported by the parasphenoid. The dorsal processes of the
pterygoids in modern Amphibia fuse with the ear capsule, while
the ventral processes may either fuse with the base of the ear
capsule or articulate with it by a joint, the old basipterygoid
joint. Primitively the pterygoid cartilage extended far forward,
fusing with the nasal capsule, and this condition still maintains
in frogs and in some primitive salamanders. In the Plethodon-
tidae the bony pterygoid which forms around the cartilaginous
element may either be missing entirely or represented by a small
nodule of bone. In Xenopus the posterior mesial borders of the
pterygoids grow caudally over the Eustachian tubes which extend
across the roof of the throat to open by a single orifice into the
pharynx. They thus form a bony protection to the tubes.
The ectopterygoid, a very primitive element which is lost early
in the history of the phyllospondyls, is still retained in some
caecilians such as Hypogeophis. As this element never appears
even as a rudiment in frogs and salamanders, it may be con-
sidered further evidence that the groups are not closely related.

The palates of modern Amphibia are remarkable in the varia-
bility of the bones which occur there. The palatine, for example,
may or may not be present within a single genus of frogs. The
urodeles are peculiar in that the prevomers and palatines fuse (at
least in part during metamorphosis), and the combined struc-
ture grows rapidly in a caudal direction in various families.
In the salamandrids (Fig. 80) two dentigerous processes of the
combined prevomers and palatine are carried back along side
of the parasphenoid, while in the plethodontids (Fig. 81), which
have been derived from the salamandrids, these two processes
overlie the parasphenoid and form a patch of tooth-bearing bone.
The prevomers may entirely disappear in some frogs, while in
others, such as Bombina, they fuse to form a single element. In
Xenopus this fusion is correlated with the reduction of the inter-
maxillary gland. The latter structure is useless in Amphibia
feeding under water, since their tongues have no need of its sticky
secretion. The palates of most frogs appear strikingly different
from those of urodeles. This is chiefly due to the long maxillae

THE SKELETON 217

Fig. 80. — Palates of a salamander and a frog showing the fundamental
resemblances in skull structure. The chief difference is that in the salamander,
Tylototriton verrucosus {A), the prevomers have grown back along either side of
the parasphenoid, while in the frog, Rana adspersa (B), these bones retain their
primitive position. Frogs are also primitive in retaining their quadratojugal
which is lost as a separate element in the urodeles. The triradiate pterygoid is
an inheritance from Carboniferous ancestors. Ex. Oc, exoccipital; Mx., maxilla;
P .Mx., premaxilla; Ps., parasphenoid; Pt., pterygoid; P. Vo., prevomer bearing
the vomerine teeth; Q.J., quadratojugal.

218

THE BIOLOGY OF THE AMPHIBIA

and short prevomers of frogs. Primitive salamandrids with
long maxillae, such as Tylototriton, have palates which are
essentially like those of frogs (Fig. 80). On the other hand,
Ascaphus, some species of Scaphiopus, and various other Salientia
may lack the quadratojugal and hence have a skull outline
resembling that of the salamandrid, Pachytriton, closely.

A B

Fig. 81. — Palates of a frog and a salamander with reduced maxillae. In most
salamanders the maxillae fail to reach the quadrate and a quadratojugal is
missing. In some frogs, such as Ascapfius truer (A), the same condition
maintains. Salamanders also specialize in the backward growth of the vomerine
bones. In the plethodontids, the posterior processes of these may become
separated as the two dentigerous patches shown in Plethodon glutinosus (B).
C.Pt., cartilaginous pterygoid; Mx., maxilla; P.Mx., premaxilla; Ps., para-
sphenoid; Pt., pterygoid; P.T., palatine tooth patches; P.Vo., prevomer; Qu.,
quadrate; Vert. I., first vertebra.

With the flattening of the skull and the widening of the inter-
pterygoid vacuities, the pterygoid underwent considerable change
in form. A row of bones which formed a dorsal cover to the
palatoquadrate bar of osteolepids and probably represented the
metapterygoid and mesopterygoid of teleosts was reduced in
the first tetrapods to a single bone. This bone articulated with

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219

the basipterygoid process and extended dorsally separating the
various branches of the fifth cranial nerve. It was handed on in
nearly this form to the reptiles where as the epipterygoid or
columella cranii, it is a characteristic element of the lacertilian
skull. In the cynodont ancestors of the mammals the epiptery-
goid became greatly broadened and finally incorporated into the
skull of mammals as the alisphenoid (Gregory and Noble, 1924).
The epipterygoid was not destined to such an important future in
the amphibian series. In the labyrinthodonts it grew larger and
developed a process which gained attachment at the prootic.
It very soon failed to separate from the pterygoid as a distinct
bone and was handed down to modern forms as an ascending

Fig. 82.- — Chondrocranium of Ichthyophis glutinosus from a model. Cart.M.,
Meckel's cartilage; Ep., epipterygoid; Pal., palatine cartilage; St., stapes; Qu.,
quadrate. {After Winslow.)

process on the palatoquadrate bar of the larvae (Fig. 82). It
is reduced or disappears on metamorphosis in both Caudata and
Salientia, and is obscured by secondary bony growths in the
adult caecilians.

Changes in the Jaws. — In the development of the skull of
urodeles many of the dermal bones of the mouth seem to arise
in part by the fusion of the bases of the teeth. This has been
interpreted as a harking back to the condition of the first bony
fish in which the dermal bones were believed to have arisen by
the fusion of the bases of placoid scales. There is no proof of
this interpretation in the immediate fossil ancestors of the
Amphibia. In the Salientia the bones arise much earlier than
the teeth. It would seem that the immediate cause for the devel-
opment of dermal bones from tooth bases in the Caudata was the
early need for teeth and tooth supports in the young carnivorous
larvae.

Perhaps the greatest reduction in the phylogeny of the amphib-
ian skull occurred in their jaws. The Embolomeri inherited a

220

THE BIOLOGY OF THE AMPHIBIA

complex mandible of ten pieces. This number is reduced in
labyrinthodonts and branchiosaurs until the extreme condition
of only a dentary and a prearticular are left in the Salientia. In
the most primitive urodeles, the Cryptobranchoidea, there is
not only a dentary, prearticular, and articular, but also an
angular. Single coronoids occur in the larvae of most urodeles
(Fig. 83) and these may be cited as another example of a primi-
tive character in these forms. The caecilians, which are primi-

Fig. 83. — The jaw of a labyrinthodont and a urodele compared from the
lingual aspect. The jaw of the labyrinthodont contains many more bones than
the jaw of the urodele. A. Eogyrinus attheyi (after Watson, Phil. Trans. Roy.
Soc. London, 1926). B. Necturus maculosus. Ana., angular; Cart.M., Meckel's
cartilage; Cor. I., coronoid I.; Cor. II., coronoid II; Cor.III., coronoid III; Den.,
dentary; P. Art., prearticular; Po.Sp., postsplenial; Sp., splenial.

tive in most features of their skulls, exhibit an early fusion of the
jaw elements. Possibly coronoids are present as well as dentary,
articular, and prearticular, for many genera retain two rows of
teeth in the lower jaw even in the adult. The anterior end of
Meckel's cartilage ossifies as a pair of distinct elements in many
Salientia even in such primitive genera as Ascaphus and Alytes.

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221

Often these symphysial bones are fused to the dentary in
Salientia, and they are hardly recognizable or absent in the
Pipidae. Their loss in certain species of this family is correlated
with a fusion of the premaxillary bones and a modification of the
respiratory mechanism characteristic of most Salientia. The sym-
physial bones seem to have developed in connection with the
special function of the premaxillae in closing the nostrils. But
it is also possible that they owe their existence as separate
elements to their occurrence in the larva, where they form the
definitive lower jaw. It may be noted, however, that a mental
bone occurred in certain osteolepids (Watson, 1926).

Auditory Apparatus. — Another part of the skull which was
closely correlated with function is the auditory apparatus and
here we cannot expect to find the progressive evolution seen in
some other parts of the skull. The primitive labyrinthodont as
represented by Eogyrinus did not transmit the sound wavea
to a fenestra in the ear capsule. It had a stapes, the fish hyo-
mandibular, but this abutted against the otic capsule. This
crude mechanism was improved early in the history of the
Labyrinthodontia. A fenestra ovalis for the proximal end of the
stapes was formed in the capsule. The stapes in some laby-
rinthodonts, as Eryops, seems to consist of two parts, the inner,
the hyomandibular; the outer, the symplectic of fishes. Some
Rachitomi, Dissorhophus, and Cacops, specialized in surrounding
the tympanum by a bony downward growth of the tabular.
The modern Amphibia exhibit a considerable range of variation
in their auditory apparatus. In many Salientia the tympanum
is hidden under the skin and in a few it may disappear altogether.
The stapes also may become greatly reduced, and in some forms,
such as Ascaphus, it may be lost. In the urodeles the auditory
apparatus is considerably modified from the primitive condition
seen in some frogs and fossil Amphibia. The tympanum and
middle ear are lost in all urodeles and the stapes becomes con-
nected with the squamosal in the larvae. Here, as a result,
the sound waves are transmitted to the quadrate from the
lower jaw when that rests on the bottom of the pond, thence are
carried to the stapes, and finally to the inner ear.

As discussed in another chapter, this apparatus is further
modified in the adult. A piece of the otic capsule, the oper-
culum, may form a footplate for the stapes in some species,
but this is apparently not the primitive condition. In primitive

222

THE BIOLOGY OF THE AMPHIBIA

frogs (van Seters, 1922) and in caecilians (Peter, 1898) the
operculum arises free of the capsule in the membrane closing the
fenestra ovalis. An opercular muscle stretches from the supra-
scapula to the plate and is said to transmit vibrations from the
forelimb to the inner ear of the metamorphosed animal. The
muscle, which may be homologous with the stapedial muscle
of Amniota, strongly suggests that the operculum originally
belonged to a movable visceral arch (Goodrich, 1930). In
which case the capsular origin of the operculum is a secondary
modification. In modern urodeles fusions between operculum
and stapes and between operculum and otic capsule is a matter
of systematic importance (Reed, 1920; Dunn, 1922).

Although the operculum may undergo various modifications
during phylogeny, other features of the urodele auditory appara-
tus may be more conservative. The columella and ceratohyal
of the urodeles chondrify out of a single blastema (Kingsbury and
Reed, 1908). Very early the columella forms an attachment to
the squamosal and not to the quadrate as in caecilians. This
is very suggestive of the conditions in labyrinthodonts from which
the branchiosaur ancestors of urodeles and frogs were evolved.
As shown by Sushkin (1927), the columella extends not downward
to the laterally placed quadrate but upward to make an articula-
tion by its suprastapedial process with the parotic crest. This
columella was apparently equipped with a cartilaginous outer
section which was in contact with a tympanum. Its inner
portion was perforated by a stapedial artery as in caecilians.
Frogs approach the first tetrapods in their otic equipment more
closely than the other modern Amphibia do. A special feature
is the tympanic annulus, a ring of cartilage surrounding the
tympanum. This develops from the quadrate and does not
seem to have a homologue in the otic apparatus of fossil forms.
Modifications of the otic apparatus occur chiefly in aquatic or
burrowing forms. In the aquatic Pipidae the tympanum lies
under the skin and the Eustachian tubes open by a common
orifice in the roof of the pharynx as in crocodiles.

Visceral Skeleton. — The visceral skeleton of modern forms
seems to be very erratically modified. A closer study, however,
reveals certain trends of evolution which may be noted here. If
we compare the loosely hung jaws of the modern fish with the
firmly attached ones of the Amphibia, it would seem that an
enormous change must have taken place in these structures in

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223

the transformation of fish into tetrapods. A comparison of the
jaws of the embolomerous amphibian with those of the osteolepid
fish shows, however, that the change was actually a slight one.
In both fish and tetrapod the upper jaw was firmly attached to
the anterior part of the neural cranium. Laterally it was securely
held by the maxilla, while mesially the basipterygoid process
formed a strong support. In both groups the posterior jaw
elements were freed for other functions; namely, the transmission
of sound waves to the otic capsule. A very similar but purely
convergent transformation occurred again in the origin of mam-
mals from cynodont reptiles. In these forms the dentary found
a new point of articulation for the lower jaw and left the posterior
jaw elements free to be changed into the otic ossicles or sound
transmission device of the Mammalia.

The visceral arches of the osteolepid fish consist of the mandib-
ular, hyoid, and five branchial arches. The jaws of osteolepid
and primitive labyrinthodont were almost identical but the
hyoid arch differed slightly. Here the hyomandibular had
already been changed into a stapes and had not only shifted its
position relative to the otic capsule but also, according to Watson
(1926), had split its proximal end into two parts, the upper of
which retained the original position of the hyomandibular, while
the lower moved down to the position of the future fenestra
ovalis. Such a bifid head of the stapes is seen in modern reptiles.
Thus, in the stapes, as in many features of the skull, we must
look to the reptiles for more primitive conditions than exist in
modern Amphibia. The Salientia in retaining a tympanic
membrane and long columella are far less specialized than the
urodeles, but neither are so primitive in this respect as the
reptiles. The columella of Rana, at least, develops independ-
ently of the hyoid. The Eustachian tube also has a specialized
mode of development. Hence, again we must rely on our
palaeontological rather than on our embryological record for an
understanding of the origin of these structures.

Since the gill arches in the adult urodele or frog are modified by
reduction and fusion, the larval branchial arches have been
considered more primitive. Gill arches of larval Branchiosauria
and Rachitomi approach those of larval urodeles in form. It is
highly probable that all groups of Amphibia, at least above the
Rachitomi, primitively passed through a larval life in the water.
At least one rachitomous form, Dwinasaurus, already in Permian

224

THE BIOLOGY OF

THE AMPHIBIA

Fig. 84. — A comparison of three stages in the ontogeny of the hyobranchial
skeleton of Hynobius (A, C, and E) with the same structure in the adults of three
other urodeles. The hyobranchial skeleton of Siren (B) is essentially that of an
early larva, while the skeleton of Megalobatrachus (Z>) represents a partly
metamorphosed condition. The hyobranchial of the adult Triturus (F), while
fully metamorphosed, is more specialized than that of the adult Hynobius.
B1-2, branchial arches I and II; Ci— 2, copular series; C61-3, ceratobranchials I
to III; Ch, ceratohyal; C.PL, copular plate; Ebi-4, epibranchials I to IV; Eh.,
epihyal; H, hyoid; T., os thyreoideum. (A, C, and E after Tsusaki, B after
Fukuda; not drawn to the same scale.)

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225

times had become neotenous. The presence of gill arches in
this form is not an indication of its lowly phylogenetic position
but merely a proof that almost at the base of the Amphibian
stem some forms began to fail to complete their development.
Gilled adults have not " secondarily returned to the water"
but have failed to leave their habitat of infancy for the reason
that their adult structures have failed to develop (Fig. 84). The
gill arches of Dwinasaurus were of the same number and had the
same arrangement as those of larval ambystomids.

The condition of the branchial arches in the metamorphosed
labyrinthodont is unknown, and it is idle to speculate as to the
steps by which the gill arches of the osteolepids were changed into
those of the first metamorphosed tetrapods. Can we in this
case resort to the embryological record as a possible guide? All
larval urodeles and Salientia have from three to four branchial
arches, while the metamorphosed adults have no more than two.
This is correlated with the change in function, more arches being
necessary to support the clefts than to give attachment to tongue
muscles. At metamorphosis the posterior arches are not merely
lost and the anterior ones shifted to the final position. As Smith
(1920) has shown, the process involves degeneration of other
parts of the visceral skeleton and the formation of much new
tissue. Whether the first tetrapods on metamorphosis underwent
such a revolutionary change in their branchial arches is unknown,
but it is highly probable that in this case as with all other meta-
morphic processes, the change was originally a very gradual one.

The hyobranchial skeleton of the adult Amphibia exhibits
considerable variety of form. In the hynobiid salamanders and
in most frogs the hyoid arches are long and continuous with the
basihyal or copula. In most urodeles the lateral portions of
the hyoid arches (epihyals) are free from the basihyal, which may
be carried far beyond the mouth when the tongue is protruded.
In these forms the basihyal, or copula, may bear one or two
pairs of cornua. Some urodeles, especially Ambystomidae,
possess an arcuate bar in the floor of the pharynx connecting one
pair of cornua. In many urodeles the posterior part of the
copular piece of the larval hyobranchial separates on metamor-
phosis from the remainder of the apparatus and ossifies as a
distinct os thyreoideum lying cephalad to the pericardium.
Neither of these modifications is found in the hyobranchials of
other Amphibia.

226

THE BIOLOGY OF THE AMPHIBIA

The perennibranchs possess a hyobranchial apparatus which
is essentially larval, although a partial metamorphosis occurs in
this structure in Megalobatrachus. Amphiuma and Necturus
exhibit various reductions which do not appear to be metamor-
phic (Noble, 1929). The hyobranchial apparatus of the adult
caecilians consists of a single hyoid and first branchial arch
fused and followed by two or three separate branchial arches.
This retention of the branchial arches in adult life may be
considered a neotenous feature in caecilians but it may also be
correlated with the poor development of the tongue musculature
in this group. In the adult Salientia the hyobranchial apparatus
consists of a cartilaginous plate bearing three or four pairs of
processes. The most anterior pair, the hyoids, are long and
slender. They extend posteriorly and make attachment to the
skull, a secondary modification. The most posterior, the thyroid
processes, are usually well ossified and support the larynx.
Although some of this apparatus is derived from the larval
hyobranchial, part of it arises de novo. In the Pipidae the
reduction of the tongue and elaboration of the lungs and bronchus
have led to the development of a boxlike hyobranchial apparatus
with a loss of the hyoid (Ride wood, 1898), in at least one genus
(Pipa). Other changes in the structure of the hyobranchial
apparatus of adult Amphibia may have a phylogenetic rather
than a functional significance. For example, the Hynobiidae
retain two epibranchials after metamorphosis, while other sala-
manders have only one (or the barest rudiment of the second).

Laryngeal Skeleton. — The modern Amphibia have the laryn-
geal cartilages more or less specialized. In forms provided with a
voice the laryngeal cartilages would in all probability be well
developed. The presence of a tympanum in the first tetrapods
suggests that they may have used their voice to attract the
females as do modern frogs. A larval larynx is not necessarily
a primitive one. How closely the larynx of the first tetrapods
approached that of the most primitive frogs is unknown. The
form of the larynx in modern Amphibia is sometimes of systematic
importance as, for example, in the Pelobatidae (Beddard, 1907).

Vertebrae. — In the classification of the Labyrinthodontia, the
form and composition of the vertebrae as stated in Chap. I are
of primary importance. The vertebrae also present diagnostic
characters for the classification of various other major groups of
Amphibia, and hence their evolution may be considered in some

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227

detail. The vertebrae of some modern fish, such as Amia, are
embolomerous in part, in that a single neural arch is associated
with two centra in each segment. The same was true of some
of the vertebrae of the crossopterygian fish, Eusthenopteron,
which stood near the main line of tetrapod evolution. The
development of the vertebrae in Amia shows that each is formed
by the ossification and growth of four pairs of arch cartilages as
well as by an ossification in the perichordal sheath. The carti-
lages are formed from mesenchyme which condenses in the
region of greatest strain, namely the point where the myosepta,
which are under muscular pull, join the relatively stiff notochord
at its upper and lower surfaces. Thus on each side of the body
four blocks of cartilage develop, pressed against each myoseptum
at its junction with the notochord, the two anterior blocks of
each side belonging to one myotome and the two posterior, to
another. The four pairs of blocks together with what ossification
may occur in the sheath around the notochord form the basis
of a single vertebra which lies with its midpoint between two
myotomes. The cartilaginous blocks, or arcualia, have been
given names by Gadow. The pair lying in the posterior part
of one myotome and above the notochord are the "basidorsals."
The pair immediately below them are the "basiventrals." The
arcualia formed in the anterior part of a myotome and above the
notochord are the "interdorsals," those below them the "interven-
trals." Each vertebra is formed by the union of the basidorsals
and basiventrals of one segment with the interdorsals and inter-
ventrals of a posterior one.

In the Embolomeri at the very base of the amphibian phylum
each neural arch was provided with two centra. The anterior
centrum apparently represents the basiventral which has grown
dorsally and, possibly uniting with an ossification in the perichor-
dal sheath, formed an amphicoelous disc. The posterior centrum
apparently represents the interdorsal and interventral fused or
united by an ossification of the perichordal sheath to form a
similar disc.

In the evolution of the Labyrinthodontia a gradual weakening
in the ossification of the skeleton occurred. The Rachitomi,
being a step in advance over the Embolomeri, have failed to
ossify the perichordal sheath of the vertebrae completely, with
the result that the four arcualia (Fig 85B) or cartilaginous
blocks remain more or less separate on ossification. Each basi-

228

THE BIOLOGY OF THE AMPHIBIA

ventral side may fuse with its mate of the opposite to form a
moon-shaped element which, unfortunately for the sake of

Fig. 85. — Three types of vertebrae characteristic of extinct orders of Amphibia,
viewed from the left side. These types also represent stages in the progressive
reduction of ossification in phylogeny: A. Cricotus, an embolomerous labyrin-
thodont. B. Eryops, a rachitomous labyrinthodont. C. Branchiosaurus, with
epichordal vertebrae. (After Whittard.) I.C., intercentrum; N.A., neural arch;
Not., notochord; P.C., pleurocentrum; R. , rib.

clarity, is called an " intercentrum.' ' The interventrals, which
ossify free of the other elements, are called u pleurocentra,"

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229

while the interdorsals, which are of rare occurrence, are described
as "dorsal pleurocentra." In the sturgeon, Acipenser, where the
ossification of the skeleton is poorly developed, these four pairs
of blocks remain cartilaginous and illustrate in a diagrammatic
way the cartilaginous basis of the vertebrae of all back-boned
animals. The vertebrae of the Rachitomi represent an ossifica-
tion of these blocks. In most cases, there is, in addition, a fusion
of the basiventrals and a loss of the interdorsals.

In the Stereospondyli the pleurocentra, that is, the interdorsal
and interventral, are reduced or lost. It is possible that they
remain cartilaginous. The single centrum of these labyrintho-
donts probably includes a perichordal ossification as well as the
basidorsal and basiventral, but this is only an inference based on
the development of recent forms. Reptiles, which sprang from
embolomerous Amphibia, have emphasized the interdorsal and
interventral elements at the expense of the basidorsal and basi-
ventral, an arrangement exactly opposite to that of the Amphibia.

In the lepospondyls and phyllospondyls it is impossible to
determine how much was formed by arcualia and how much by
perichordal sheath. It seems probable, however, that the inter-
dorsal and interventral were reduced to cartilaginous rings
between the centra, the latter being formed from perichordal
sheath together with some contribution from the basidorsal and
basiventral. This reduction of the interdorsal and interventral
brings the rib to an intervertebral position, and this may be
considered the primitive position for the rib in the lepospondyls.
In all phyllospondyls the rib has shifted to the side of the vertebra
and is attached to a well-marked transverse process. The verte-
brae of frogs and salamanders agree in the extensive development
of the perichordal ossification, the basidorsal and the basiventral
being intimately associated with it in their ossification. Primi-
tive frogs, the Liopelmidae, agree with primitive urodeles in that
the interdorsal and interventral remain cartilaginous throughout
life ; the vertebrae are thus amphicoelous, as in lepospondyls and
some phyllospondyls. In Ascaphus these cartilaginous rings
serve to hold the vertebrae together and no joint surfaces are
formed. In higher frogs and urodeles this cartilaginous ring or
ball splits in such a way that most of the cartilage is either on
the anterior or the posterior end of a vertebra. When the
cartilage ossifies an opisthocoelous or a procoelous vertebra
results, according to whether the ball is on the anterior or the

230 THE BIOLOGY OF THE AMPHIBIA

posterior end of the centrum. In a few pelobatid and bufonid
toads the ball ossifies but remains more or less free from the
centra on either side of it. This ossification of the inter dorsal
and interventral cartilages is an advance in vertebral evolution
not found in either lepospondyls or, at least in its typical form, in
phyllospondyls. Except for this feature the vertebrae of modern
Amphibia agree closely with those of these extinct orders.

The development of a vertebra does not always give a clear
picture of its phylogenetic origin. Thus, in Rana the basidorsals
appear but soon fuse to form two longitudinal strips along the
upper surface of the notochord. A similar cartilaginous strip
which develops along the ventral side of the notochord produces
regular swellings. These have been homologized with fused
basiventrals and interventrals. Ingrowths of the dorsal cartilagi-
nous strips begin to constrict the notochord and the ossification
beginning in them spreads round the notochord in the perichordal
sheath. Cartilage, apparently representing the inter dorsals,
early appears intervertebrally and when it ossifies forms a ball
which may remain attached to the centrum either before or
after it. Most vertebrae in Rana are procoelous, that is, the
ossified intervertebral cartilage remains attached to the centrum
anterior to it. In the coccygeal region the three longitudinal
strips of cartilage never split into distinct vertebrae but ossify
to form a rodlike bone, the coccyx or urostyle.

In the primitive Discoglossidae, Pipidae and Pelobatidae, the
perichordal sheath may not ossify, and when the notochord is
reduced on metamorphosis, vertebrae are produced with greatly
flattened centra. It seems probable that branchiosaurs had the
same type of vertebrae (Fig. 85, C). The Gymnophiona, which
have been found to be so primitive in various features of their
skull and vertebrae, might be expected to afford a primitive type
of vertebral development. Marcus and Blume (1926) have
followed the development of the vertebrae of Hypogeophis.
Gadow's four pairs of arcualia appear, but the basidorsal and
interdorsal fuse to form the neural arch, the intervertebral
cartilage which is poorly developed arising from the ventral
arcualia. Even in this primitive group, cartilaginous strips
appear before the arcualia and take part in their formation.
Marcus and Blume have showed that similar parachordal carti-
lages appear in other vertebrates, although their homology with
the early cartilage strips in frog vertebrae is not clear. An

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231

important feature in the ontogeny of Hypogeophis is the retention
of the early embryonic metamerism in the ventral arcualia.
While the basidorsal of one segment unites with the interdorsal
of the succeeding to form the neural arch, the basiventral and
interventral of the first segment form the ventral arch of the
resulting vertebra. Possibly the Lepospondyli, with ribs inter-
vertebrally situated, have vertebrae which developed the same
way. Since this can never be determined in these fossil forms,
it is impossible to say how closely the lepospondyls agree with
the Gymnophiona in the composition of their vertebrae.

The number of vertebrae ranges from over 200 in some caecil-
ians to only 6 segments in the Roraima toad, Oreophrynella, and
in the African Hymenochirus of a very different family. In
the latter, more than in the former, the composite nature of
the sacrum is indicated by its great length. Hymenochirus is
thoroughly aquatic, while Oreophrynella is terrestrial, and hence
this reduction in the number of vertebrae is not correlated with a
special type of habitat. The number of vertebrae may be
reduced by a fusion of the first and second vertebrae as in some
species of Xenopus and of Atelopus. Salientia have fewer
vertebrae than Caudata. The most primitive family of frogs,
the Liopelmidae, have one more presacral vertebra than any other
Salientia. The pelvis may attach to any one of a great number
of vertebrae. Thus, in Amphiuma there are 63 vertebrae exclu-
sive of the caudals, while in the more primitive, shorter-bodied
urodeles this number of dorsal vertebrae is usually less than 20.
The increase in number of vertebrae may continue during life.
In a small but fully formed Batrachoseps attenuatus 2.3 cm. from
snout to vent, I find there are 22 dorsal vertebrae and 28 caudals,
a number which approximates that found in some species of
Plethodon. In an adult 4.75 cm. head and body length, there
are 22 dorsals and 61 caudals. Hence, the number of tail verte-
brae more than doubles during the active terrestrial life of this
species. The frogs and toads are characterized by the reverse
phenomenon, namely, the reduction of the tail during ontogeny.
Correlated with this reduction, the caudal cartilages fuse to
form a bony rod, the coccyx. In the Discoglossidae the diapophy-
ses of the first of these coccygeal vertebrae are formed as small
but discrete elements. The number of potential vertebrae taking
part in the formation of the coccyx is difficult to estimate, for a
separation is indicated during ontogeny in only two or three of

232

THE BIOLOGY OF THE AMPHIBIA

the more anterior ones. The caudal vertebrae of urodeles are
much more primitive. They are provided ventrally with a series
of processes, the haemal arches. As shown by Gamble (1922),
these arise like the parapophyses as a pair of processes from the
basiventrals. In the trunk region the parapophyses enlarge,
while in the tail region the haemapophyses dominate, the para-
pophyses disappearing.

The first vertebra of the column is modified for articulation
with the skull. It is cup-shaped without transverse processes
but with two facets for the occipital condyles. There is no
atlas-axis complex as in higher vertebrates for the rotation of the
head. In many Caudata there is an anteriorly directed process
on the first vertebra, however, which bears a pair of additional
facets. This process may represent a part of a vertebra, the
neural arch of which has been lost.

Ribs. — The ribs in primitive Amphibia were long and tended
to surround the body like a series of hoops. They articulated
with the vertebrae as far as the middle of the tail. The ribs are
genetically closely related to the various processes of the verte-
brae; namely, diapophyses, parapophyses, haemapophyses, and
rib bearers. Unlike these processes they usually arise in the
septa at a distance from the notochord and later gain an
articulation with the vertebrae. With the shifting of the hori-
zontal muscle septum, the ribs come to lie higher on the vertebrae
and thus the parapophyses may gradually change into the dia-
pophyses. The ribs were primitively single-headed but even in
some Embolomeri they have become two-headed. The lower
head, or capitulum, articulates principally with the basiventral,
while the upper head, or tubercle, abuts against the basidorsal.
The ribs of Gymnophiona, when they first appear in ontogeny, are
continuous with the vertebrae. Since the capitulum apparently
is derived from the ventral arcualia, the tubercle from the dorsal
arcualia, Marcus and Blume (1926) have assumed the two-headed
condition of the rib primitive. The septum in which the rib
rises may change its relationship to the vertebrae and hence vari-
ous shiftings of the ribs have occurred during phylogeny. Thus,
within the lepospondyls the vertebrae either may have the primi-
tive intervertebral position or may articulate with diapophyses
extending from the side of the arch. Both frogs and salamanders,
since they arose from the typical branchiosaurs, presumably
had their ribs attached to stout diapophyses. This condition is

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233

retained in the frogs. A very similar condition is found in hyno-
biids and cryptobranchids. In most urodeles the ribs are two-
headed and attach lower on the side of the vertebrae than in
frogs. In a single animal, such as Necturus, the capitular head
of the ribs shifts from a parapophysis, or process from the side
of the centrum in the vertebrae of the trunk region, to a ribbearer,
a more dorsal process of the second and third vertebrae (Gamble,
1922). This division of a rib head into a capitulum and tubercle
may have originated within the Caudata. At least it is not found
in frogs and reaches its greatest development in the more special-
ized urodeles. The functional significance of double-headed
ribs would seem to lie in their mechanical advantage over single-
headed ones in resisting the downward pull of the viscera in
terrestrial life.

Although the ribs are long in some labyrinthodonts and lepos-
pondyls, they never meet in the midline or take part in the forma-
tion of the sternum. In the branchiosaurs the ribs are short and
straight, and this condition is inherited by frogs and salamanders.
It is sometimes assumed that the ribs of Amphibia are duplex
structures which have arisen by the fusion of the dorsal and
ventral ribs of fishes (Naef, 1929). Although there is no reason
why the rib-forming mesenchyme may not shift its position in
the septa, there is no palaeontological proof of this fusion of
dorsal and ventral ribs in the ancestors of modern Amphibia.

In the primitive salamandrids, such as the Spanish newt,
Pleurodeles waltl, and also in its close relative, Tylototriton, the
tips of the ribs may be pointed and actually protrude through
the skin. This modification of the ribs finds a parallel in the
toes of some African frogs where the terminal phalanges protrude
through the integument. The modification in the urodeles is
believed to serve as a mode of protection.

In the more long-bodied salamanders, such as Siren and
Amphiuma, the ribs are greatly reduced in number and are
found only on the anterior vertebrae. In the Salientia the
reduction has reached an extreme; only the liopelmids and
discoglossids retain ribs in the adult, but the pipids have
ribs while larvae. These ribs in the pipid larvae later fuse
to the diapophyses of the vertebrae and are not distinguish-
able from them. No ribs appear as distinct ossifications in
Salientia higher than the Pipidae, although bits of cartilage
are frequently found on the ends of the diapophyses.

234

THE BIOLOGY OF THE AMPHIBIA

Abdominal Ribs. — The ventral side of the body of many
Labyrinthodontia, Lepospondyli, and especially Phyllospondyli
was sheathed with a coat of closely set bony rods or plates. These
had various forms and sizes but they were usually arranged in a
series of /\-shaped rows, with the apexes directed forward.
They are unknown in the Stereospondyli and may have been lost
in other higher Labyrinthodontia. The reptiles inherited their
abdominal ribs from embolomerous ancestors. The turtles
fused some of them together to form part of the plastron. Sphe-
nodon and some lizards retain them as slender rods of cartilage
or bone in the ventral musculature (see Camp, 1923).

The abdominal ribs were well developed in the branchiosaur
ancestors of the Caudata and Salientia. Large cartilages of
much the same form as the abdominal ribs of the lizards appear
in the myosepta of the M. rectus abdominis of Liopelma (Fig. 94).
Goette found in Bombina some traces of paired cartilage forma-
tion in the ventral musculature which, according to Gegenbaur,
might correspond to the ventral sections of true ribs. The
abdominal ribs, however, have no ontogenetic nor phylogenetic
relationship to the true ribs. They are dermal elements similar
to the interclavicle in origin. The development of these slips
of cartilage in the Liopelmidae and Discoglossidae has not been
studied. In their adult condition they appear to be remnants
of the abdominal basket of the branchiosaurs. Similar pieces
of cartilage have been described in Necturus, but in no urodele
are they so well developed as in Liopelma.

Pectoral Girdle. — The pectoral girdles of frogs and salaman-
ders appear very different, although they both were derived from
the same type originally. The Embolomeri inherited a girdle
almost exactly like that of their fish ancestors except that a new
element, the interclavicle, was added to its ventral surface. The
girdle consisted of two half rings articulating in the midventral
line with the interclavicle. The bulk of each half ring was formed
by a single element, the scapula or scapulo-coracoid, for in the
higher Amphibia there are two centers of ossification in this
element. On the anterior edge of the scapulo-coracoid were a
clavicle and a cleithrum as in fish. In the most primitive
Embolomeri there were also a supracleithrum and a post-temporal
attaching the clavicle to the skull.

Within the Labyrinthodontia there occurred an increase in the
size of the scapulo-coracoid element at the expense of the dermal

THE SKELETON 235

Fig. 86. — The pectoral girdles of three orders of Amphibia showing a progres-
sive loss in the bony elements and an increase in cartilage. A. Eryops, a labyr-
inthodont {after Miner). B. Ascaphus, a primitive frog. C. Amby stoma
jeffersonianum, a salamander. CI, clavicle; Cor., coracoid; Cor. Car., coracoid
cartilage; Cth., cleithrum; Gl., glenoid; Id., interclavicle; P. Cor., procoracoid;
S.Sc, suprascapula; Sc., scapula; Sc.Cor., scapulo-coracoid; St. sternum.

236

THE BIOLOGY OF THE AMPHIBIA

elements. In the Rachitomi the connection with the skull was
lost, but in the more terrestrial members of the same group the
girdle shifted so near to the base of the skull that there could have
been little movement of the neck. The formation of the double
occipital condyle further strengthened the skull against side move-
ments. In the more advanced labyrinthodonts of undoubted
aquatic habits there occurred a broadening of the ventral ele-
ments. The loss of the clavicle, interclavicle, and cleithrum in
the urodeles (Fig. 86) may have been correlated with continued
aquatic habits, possibly also with the greater development of
movement in the forelimbs. The branchiosaurs afford a valuable
clue to the origin of the distinctive features of the pectoral girdle
of modern Amphibia. Not only their coracoids but the entire
glenoid region was unossified. They still retain a very narrow
clavicle and cleithrum and usually a small interclavicle while
specializing in the development of a broad cartilaginous coracoid.
The urodeles merely extend this condition one step further; they
lost the dermal elements and further broadened the coracoid.

The primitive Salientia approach the branchiosaurs even more
closely in the form of their pectoral girdle, the chief difference
being that the posterior part of the coracoid cartilage became
ossified as a distinct piece, while the glenoid extended its
ossification into the procoracoid region in some forms (Liopel-
midae). The main part of the cartilaginous ventral plate of the
branchiosaurs remained unossified anteriorly to form the so-called
" procoracoid cartilage" (Fig. 86). It is interesting to note that
two salamanders, Siren and Pseudobranchus, have also developed
an ossification in the posterior half of the coracoid plate. This
must be considered a change parallel to that of frogs. The dorsal
end of the scapula frequently calcifies in Salientia, and it may
ossify as a suprascapula, which is not to be confused with the
cleithrum in the same region. Urodeles are peculiar in the great
dilation of the coracoid cartilage and in the extension of the ante-
rior process, the so-called " procoracoid." The two halves of the
girdle overlap in the midline and this is doubtless a primitive
inheritance.

Within the Salientia many modifications of the pectoral girdle
take place. In various families the two halves may fuse in the
midline (Fig. 87), forming the firmisternal type of girdle as
distinguished from the more primitive arciferal type where the
two halves merely overlap. Within a single family, the Brevici-

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237

pitidae, both clavicle and procoracoid may become lost entirely.
An anterior extension of the procoracoid cartilage in the midline
frequently splits off to form a
distinct element which may
become ossified. This is the
so-called "omosternum,"
which in some families, espe-
cially in the Polypedatidae and
African Ranidae, may become
widely forked posteriorly.
The sternum is a cartilaginous
plate in primitive frogs, and
since a sternum is never found
among the fossilized remains
of branchiosaurs and labyrin-
thodonts, it may have been
represented by a cartilaginous
piece in these ancestral groups
as well. In primitive frogs
the sternum resembles the ab-
dominal ribs but possesses
anteriorly two leaves fitting
between the coracoid carti-
lages. In the higher Salientia
these leaves are lost and the
diverging processes of the
sternum fuse to form a single
plate which in the many ad-
vanced types may become
ossified. The sternum of the
discoglossids resembles that of
urodeles, while that of many
higher Salientia is specialized
not only by calcifying or ossi-
fying but also by assuming a
plate or rodlike form. The
narrow, bony sternum of Rana
represents the extreme condi-
tion of this modification.

Pelvic Girdle. — The pelvis of the primitive Embolomeri was a
distinct advance over the condition found in any fish. It was

Fig. 87. — The pectoral girdles of three
neotropical frogs showing the change from
the arciferal to the firmisternal type. A.
Eleutherodactylus bransfordii. B. Smin-
thillus limbatus. C. Rhinoderma darwinii.

238 THE BIOLOGY OF THE AMPHIBIA

Cocc*

pre-pub.

post- pub.

Fig. 88. — The pelvis of a frog and that of a salamander compared. A. Pelvis
of Ascaphus truei viewed laterally. B. Same seen from below. C. Ventral
aspect of pelvis of Tylototriton verrucosus. A prepubis occurs in both. In the
salamander the pubis is cartilaginous, while in the frog it is fused with the
ischium. Cocc, coccyx; Isch., ischium; Os.il., ilium; post-pub., postpubis;
pre-pub. prepubis; Pub., pubis; pubo.isch,, puboischium; Sac, sacrum.

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239

a triradiate structure on each side with a long ilium, a short
ischium and pubis meeting in the acetabulum (Fig. 88A). The
more terrestrial labyrinthodonts had all three elements well
ossified, and such a girdle was handed on to the reptiles as a
primitive inheritance. Within the Embolomeri various changes

Fig. 89. — Variation in the sacrum of Atelopus varius. A single vertebra, the
ninth, usually forms the sacrum, but others may fuse with it.

occurred. Watson (1926) has shown that Diplovertebron
retained a cartilaginous pubis, and this condition was handed on
to the branchiosaurs and to modern frogs and salamanders.
Amphibia never have the large obturator foramen characteristic
of the pelvis of reptiles, nor do they usually ossify the pubis. In
the Salientia the pelvis is greatly compressed, and in some

240

THE BIOLOGY OF THE AMPHIBIA

species the pubis is calcined, or even ossified. The cartilaginous
pubis is, however, the primitive inheritance of both frogs and
salamanders.

Many aquatic urodeles have developed a Y-shaped cartilage
attached to the anterior end of the pubis (Fig. 88C). Whipple
(1906) has shown that this structure and its muscles serve to
control the shape of the inflated lungs which in these species act
largely as hydrostatic organs. Contraction of the muscles pulls
the cartilages dorsally, forcing the air anteriorly into the lungs
and making the head end of the animal more buoyant. It may be
noted, however, that Ascaphus, which frequents streams and has
no need of a hydrostatic organ, has also a cartilaginous plate
anterior to the pubis, and hence a prepubis may have been a
primitive character of modern Amphibia. Ascaphus has also
developed a pair of rodlike cartilages lying on the ventral surface
of the pubis of the male and serving as a support for the copula-
tory apparatus which is unique in this frog.

The pelvis of Salientia is especially characterized by its long
ilia which make a ligamentous connection with the diapophyses
of the sacral vertebrae. There may be two or three of these
pairs of diapophyses, but one is the rule. In some Salientia
these diapophyses may be greatly expanded (Fig. 89). The
functional significance of this modification is, however, not clear.
In the urodeles, sacral ribs afford a support to the ilia. The
pelvis is lacking in Siren, the caecilians, and some lepospondyls.

Limbs. — The general correspondence between the fins of fish
and the limbs of tetrapods is obvious, but the detailed record of
how the former were converted during Devonian or Silurian
times into the latter is lacking. Anatomists have, therefore,
come from time to time to the rescue of the evolutionist and have
advanced many ingenious theories as to how fins might have
changed into legs. Thus the fin supports of sharks, of lung
fishes, of Polypterus, and even the forelimb skeleton of the very
young salamander larva have been taken by the advocates of one
or the other theory as a basis for further modifications. The
difficulty with all these theories is that they are based on modern
forms, and where any palaeontological evidence is available
this should be considered first to the exclusion of all other data.

The skeletons of the forelimbs of only a few generalized cros-
sopterygians are known. These consist of a proximal humerus
and two distal elements which may be called " radius" and

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241

1 ' ulna. ' ' Distal to the latter are a series of elements too numerous
to be homologized with definite digits. The most radical change
in the evolution of the fish paddle into the forelimb of tetrapods
must have been in the reduction of elements in this distal row.
The fundamental plan of humerus, radius, ulna, and a series
of digits was marked out in the skeleton of the fish paddle long
before the tetrapods evolved (Fig. 90).

Embolomeri might have been expected to show the most
primitive type of tetrapod limb. Watson (1926) has shown

Ancestral Tetrapod

\eiical- based on Bombina Larva)

Fig. 90. — Diagram of the evolution of the carpus: c, centrale; ci_5, carpalia;
C-S, scapulo-coracoid, H, humerus; %., intermedium; medialia;Pp, prepollex;

Pm, postminimus; r, radiale; R, radius; u, ulnare; U, ulna. (After Gregory, Miner
and Noble.)

that Diplovertebron agreed with the oldest reptiles in having
five well-developed fingers and toes. On the other hand, Greg-
ory, Miner, and Noble (1923) found evidence of a prepollex
in the rachitomous Eryops, and although four well-developed
digits were present, there was space for cartilaginous pieces which
might represent a fifth and a sixth digit. It might be argued that
the short thumb of Diplovertebron represents the prepollex of
modern Amphibia, but Steiner (1921) found that in Bombina
five digits were present in the blastema of the hand as well as
the prepollex. The prepollex has also been described in the
embryo of reptiles (Steiner, 1922). Thus there can be no doubt

242

THE BIOLOGY OF THE AMPHIBIA

that the original hand consisted of a prepollex as well as five
digits and possibly also a cartilaginous rudiment of a sixth digit.
In all Amphibia above the Embolomeri, only four functional
digits are known, although some fossil types, to judge from the
tracks, may have had a supporting ray on the inner side, namely,
the prepollex. In frogs and toads the prepollex is often enlarged
in the male to serve as a gripping organ during amplexus. A
bony prepollex is, moreover, present in some salamanders such
as Amby stoma opacum. The inheritance of modern Amphibia
was, thus, a prepollex, four digits, and the rudiment of a fifth
in the hand.

Diplovertebron possessed five digits in the hind foot. In
most Salientia there are not only five digits but also a prehallux.
In some primitive salamanders there may be both a cartilaginous
prehallux and postminimus (Schmalhausen, 1910). Since the
prehallux forms the core of the " spade" in burrowing Salientia,
it is sometimes considered a neomorph. It is, to be sure, hyper-
trophied in burrowing types, but as it also occurs in non-burrowing
species it would seem to be a primitive inheritance. In the
evolution of the Amphibia there has been a reduction not only
of the number of digits but also in the number of carpal and
tarsal elements. The Rachitomi had more of these elements
than any recent form. There was a proximal row in the hand
of four elements called the "radiale," "centrale," " interme-
dium, " and "ulnare," respectively. In the foot elements hav-
ing a similar position are called "tibiale," "centrale," " interme-
dium," and "fibulare." Distal to this proximal row in hand
and foot, there was, respectively, a row of three carpal and three
tarsal elements, called "medialia" by Schmalhausen. Distal
to these were five carpalia in the hand and five tarsalia in the
foot. There was, therefore, an almost exact correspondence
between the elements in the primitive carpus and those of the
primitive tarsus.

The carpus and tarsus of modern Amphibia differ from those of
Rachitomi in exhibiting various fusions. The primitive sala-
manders approached most closely to the original condition.
Schmalhausen (1917) found that the tarsus in Ranodon differed
from that of Trematops only in that tarsalia I and II are fused.
In the Salientia marked changes have occurred in all three rows
of elements and also in the long bones of the legs. Radius
and ulna are no longer separate but fused to form a single bone

THE SKELETON

243

in each forelimb, and the fused tibia and fibula form a single
bone in each hind limb. The tarsus of the frogs is distinctive
in the elongation of the tibiale and fibulare and in the loss or
fusion of most of the other elements except a few tarsalia. The
primitive families retain three tarsalia, the more advanced only
two. The elongation of the proximal segment of the tarsus
may be an adaptation for jumping, and the reduction of the distal
elements may be a consequence of this elongation. The tibiale
and fibulare may be fused together at their two ends in some
Salientia, while in Pelodytes they are united for their entire
length. The Salientia, which are more primitive than Caudata
in most details of the skeleton, have specialized considerably
away from the primitive condition in their single lower limb
bones and in their reduced carpus and tarsus. Discoglossidae
and Pelobatidae exhibit fewer fusions than the higher Salientia
(Ridewood and Howes, 1888). The carpalia III and IV, for
example, are usually free instead of fused to the mediale III. The
medialia are always more or less fused to other carpal elements
in all Salientia, and the intermedium of urodeles never appears
in the group as a separate element.

Diplovertebron had a phalangeal formula of 2, 3, 3, 3, 4 in
the forelimb. This formula is unique, and Watson (1926)
suggests that it has arisen by reduction from the primitive
reptilian formula which was presumably found in the most
primitive Embolomeri (whose appendages are unknown). It
may be assumed that the most primitive tetrapods had a formula
of 2, 3, 4, 5, 4. The number 2, 2, 3, 4, 3, is retained in the feet
of most labyrinthodonts, at least one branchiosaur, and most
Salientia. The labyrinthodont Trematops and the lepospondyl
Hylonomus, etc., have been credited with 2, 3, 4, 4, 3, phalanges
in the foot. Most urodeles have 2 (1), 2, 3, 3, 2 phalanges in
the foot and 2 (1), 2, 3, 2, in the hand. Eryops had the same
number of hand phalanges, but most branchiosaurs and the
Salientia usually have 2, 2, 3, 3 phalanges. One branchiosaur,
however, has the typical urodele number. One group of species
of Ambystoma have redeveloped an extra phalanx in the fourth
toe, and their formula reads 2, 2, 3, 4, 2 (Cope, 1889). Whether
or not this be considered a case of atavism, it is interesting to
note that the Salientia in spite of their specialized tarsus approach
nearer to their branchiosaur ancestors in number of hind limb
phalanges than do the Caudata.

244

THE BIOLOGY OF THE AMPHIBIA

Reduction in the length of the lateral digits or the complete
loss of the same occurs in both Salientia and Caudata. Many
of these reductions have a systematic value as discussed in
another chapter. Where losses occur, the tarsal or carpal
elements are reduced apparently by fusion. In Proteus and
Amphiuma with three digits in the forelimbs, the carpus may be
reduced to three elements (Kingsley, 1925). On the other hand,
increase in length may lead to a multiplication of parts. Thus,
the prehallux of Rana hexadactyla may be divided into three
segments.

Skeleton of Modern Amphibia. — In conclusion, it may be
emphasized that the Salientia, the Caudata, and the Gymnophi-
ona represent three lines of evolution, each of which retains
primitive characters of its own. The Salientia exhibit various
primitive characters in their skull, pectoral girdle, and digits,
while the Caudata are obviously nearer the ancestral stock in
the character of their lower jaws, ribs, pelvis, carpus, and tarsus.
The Gymnophiona, although highly specialized for fossorial life,
exhibit such primitive features as an ectopterygoid and epiptery-
goid, both lost or greatly reduced by the adults of the other
orders. Thus, it cannot be said that the skeleton as a whole,
of frog, salamander, or caecilian is more primitive than that of
the other Amphibia. Another general conclusion which may
be derived from the above review is that homology must be
based upon the phylogenetic and not the embryological origin
of a structure. The limbs, sacrum, occiput, and many other
parts of the skeleton may be derived from different somites in
different groups of Amphibia. Nevertheless, if structures in
different groups can be demonstrated to have arisen from the
same structure in a common ancestor, they may be considered
homologous. Apparently, organ-forming materials may become
distributed in different somites in the course of phylogeny. We
shall refer to this subject again in the following chapter.

References

Beddard, F. E., 1907: Notes upon the anatomy of a species of frog of the

genus Megalophrys, with reference to other genera of Batrachia,

Proc. Zool. Soc. London, 1907, 324.
Camp, C. L., 1923: Classification of the lizards, Bull. Amer. Mus. Nat.

Hist., XLVIII, Art. XI.
Cope, E. D., 1889: The Batrachia of North America, Bull. U. S. Nat. Mus.,

No. 34.

THE SKELETON

245

Dunn, E. R., 1922: The sound-transmitting apparatus of salamanders and

the phylogeny of the Caudata, Amer. Naturalist, LVI, 418-427.
Edgeworth, F. H., 1920: On the development of the hypobranchial and

laryngeal muscles of Amphibia, Jour. Anat., LIV., 125-162.
Gamble, D. L., 1922: The morphology of the ribs and transverse processes

in Necturus maculatus, Jour. Morph., XXXVI, 537-566.
Goodrich, E. S., 1930: "Studies on the Structure and Development of

Vertebrates," London.
Gregory, W. K., R. W. Miner, and G. K. Noble, 1923: The carpus of

Eryops and the structure of the primitive chiropterygium, Bull.

Amer. Mus. Nat. Hist., XLVIII, 279-288.
Gregory, W. K., and G. K. Noble, 1924: The origin of the mammalian

alisphenoid bone, Jour. Morph. Physiol., XXXIX, 435-463.
Kingsbury, B. F., and H. D. Reed, 1909: The columella auris in Amphibia,

Jour. Morph., XX, 549-628, 10 pis.
Kingsley, J. S., 1925: "The Vertebrate Skeleton," New York.
Marcus, H., and W. Blume, 1926: Uber Wirbel und Rippen bei Hypogeo-

phis nebst Bemerkungen uber Torpedo, Zeitschr. Anat. Entw., LXXX,

1-78.

Naef, A., 1929: Notizen zur Morphologie und Stammesgeschichte der
Wirbeltiere; 15. Dreissig Thesen liber Wirbelsaule und Rippen ins-
besondere bei den Tetrapoden, Zool. Jahrb. Anat. AM., L, 581-600.

Noble, G. K., 1929: Further observations on the life-history of the newt,
Triturus viridescens, Amer. Mus. Novit., No. 348.

Peter, K., 1898: Die Entwicklung und funktionelle Gestaltung des Schadels
von Ichthyophis glutinosus, Morph. Jahrb., XXV, 555-628, pis. 19-21.

Reed, H. D., 1920: The morphology of the sound-transmitting apparatus
in caudate Amphibia and its phylogenetic significance, Jour. Morph.,
XXXIII, 325-375.

Ridewood, W. G., 1898: On the structure and development of the hyo-
branchial skeleton and larynx in Xenopus and Pipa; with remarks
on the affinities of the Aglossa, Jour. Linn. Soc, XXVI, 53-128, pis.
VIII-XI.

, and G. B. Howes, 1888: On the carpus and tarsus of the Anura,

Proc. Zool. Soc. London, 141-182.
Schmalhausen, J. J., 1910: Die Entwickelung des Extremitatenskelettes

von Salamandrella Kayserlingii, Anat. Anz., XXXVII, 431-446.
, 1917: On the extremities of Ranidens sibiricus Kessl, Rev. Zool.

Russe, II, 129-135.

Seters, W. H. van, 1922: Le developpement du chondrocrane d'Alytes
obstetricans avant la metamorphose, Arch, de Biol., XXXII, 373-491,
pis. 8-9.

Smith, Louise, 1920: The hyobranchial apparatus of Spelerpes bislineatus,

Jour. Morph., XXXIII, 527-550.
Stadtmuller, Franz, 1929: Studien am Urodelenschadel; II. Nachweis

eines Basioccipitale bei einem rezenten Amphibium (Triton alpestris),

Zeitschr. Anat. Entw., XC, 144-152.
Steiner, H., 1921: Hand und Fuss der Amphibien, ein Beitrag zur Extremi-

tatenfrage, Anat. Anz., LIII, 513-542.

246

THE BIOLOGY OF THE AMPHIBIA

Steiner, H., 1922: Die ontogenetische und phylogenetische Entwicklung des

Vogelfliigelskelettes, Acta Zoologica, III, 307-360.
Sushkin, P. P., 1927: On the modifications of the mandibular and hyoid

arches and their relations to the brain case in the early Tetrapoda,

Pal. Zeitschr., VIII, 263-321.
Watson, D. M. S., 1926: The evolution and origin of the Amphibia, Phil.

Trans. Roy. Soc. London, Ser. B, CCXIV, 189-257.
■ , 1926a: The Carboniferous Amphibia of Scotland, Palaeontologica

Hungarica, I, 221-252, 3 pis.
Whipple, Inez L., 1906: The ypsiloid apparatus of urodeles, Biol. Bull.,

X, 255-297.

CHAPTER XI

THE MUSCULAR SYSTEM

The Amphibia exhibit many modes of locomotion: the aquatic
urodeles have retained some of the swimming movements of
fish; the frogs have specialized in leaping and have lost the tail;
many burrowing Salientia must be content with walking, as
they are too short-legged to leap; finally, a few salamanders and
many frogs have become arboreal and can successfully clamber
up the trunks of trees. As in other animals, nearly all move-
ment in the Amphibia is produced by muscles. These are of two
kinds : the involuntary, non-striated muscle derived from the mes-
enchyme (rarely from ectoderm) and found in the walls of diges-
tive tracts, viscera, blood vessels, etc., and the voluntary, striated
muscle arising from the myotomes and serving for the movement
of limbs and body wall as well as for the attachment of many
skeletal elements to one another. The muscles of the gill arches
and jaws arise from mesenchyme in the wall of the pharynx, but
they become striated and voluntary and are spoken of as visceral
in contradistinction to the somatic voluntary muscles of myotome
origin. The heart muscles are also of mesenchyme origin.
They become striped but remain involuntary in action. Further,
they have a distinctive branching or anastomosis of fibers not
found in other muscular tissue. It is thus possible to classify
muscles in several ways: according to their origin from mesen-
chyme (visceral) or myotomes (locomotor and body muscles),
according to function (voluntary and involuntary), according to
their structure (smooth or striated), according to their innerva-
tion (facial, etc.). None of these classifications has proved
thoroughly satisfactory, since in all cases there is a certain inter-
gradation between the types. For example, limb muscles may
arise from myotomes in sharks but apparently from mesenchyme
in Amphibia. Muscle movement is caused by the contraction
of either the muscle cell itself or the contractile myofibrils
within the cell or group of cells. The voluntary muscles are
much more rapid in their action than the involuntary muscles.
They owe their speed of action to their myofibrils which are

247

248

THE BIOLOGY OF THE AMPHIBIA

striated, that is have alternate light and dark transverse segments
unlike the myofibrils of smooth muscle.

Although all muscles are under nervous control of impulses
from the central nervous system, visceral muscles may respond
directly to stretching by contracting. Further they may main-
tain a state of contraction once obtained without further nervous
stimulation. In this they stand in contrast to the skeletal
muscles which owe a sustained contraction to rapidly recurring
stimuli. With the onset of fatigue the skeletal muscles relax.
The heart continues its contractions when removed and placed in
suitable fluid; it is thus an independently functioning organ whose
activity is merely influenced by sympathetic and parasympathetic
impulses. Its rhythmic activity is due to the refractory period
following each contraction during which the heart cells are
incapable of excitation. Since the duration of this refractory
period differs with the species, the isolated hearts of different
species of Amphibia beat at different rates.

The form and arrangement of the muscles are very closely cor-
related with function. The skeleton is merely a trestle work for
the muscles which frequently may shape the form of the bones.
Since the skeleton usually affords the best evidence of a species
relationship, it is of interest to examine not only the correlation
between bone and muscle form but also the phylogenetic changes
in the muscle system as a whole, since the latter no doubt has
left its stamp upon the skeleton. The muscles of the frog are
frequently used in physiological studies and the names applied
to the separate elements are largely borrowed from human
anatomy without sufficient evidence as to the homology of the
parts. The muscular system of the frog has been derived from
that of a primitive amphibian ground plan which is not yet
known in all its details. Some of the more obvious features of
this plan may be discussed with relation to the evolution of the
Amphibia.

The muscular system of vertebrates was originally segmentally
arranged with a pair of spinal or cranial nerves to each segment.
Connective tissue sheets, or myocommata, separated the respec-
tive segments, and in Amphibia where muscles, such as the
rectus abdominis, are built out of components from several
segments, the myocommata may still remain as evidence of this
primitive segmentation. The innervation is the best evidence
of the homology of a muscle, for the original nerve supply tends
to follow a muscle throughout the various migrations it may

THE MUSCULAR SYSTEM

249

have made during phylogeny. Transplantation experiments
have shown that this relation between nerve and muscle is not a
fundamental one, since limbs transplanted into a foreign position
may pick up a new nerve supply from the spinal nerves of its
new environment (Detwiler, 1920; Mangold, 1929). Further,
just as the pelvis or the occiput may be formed from different
somites in labyrinthodonts and frogs and yet be considered
homologous structures, so the limb muscles, together with their
nerve supply, may have arisen in these two groups from dif-
ferent somites but are nevertheless considered homologous.

Body Muscles. — The somatic muscles derived from the
myotomes give rise to the trunk muscles and in other groups after
modification to the limb muscles, while in the gill region they
are squeezed into an epibranchial and a hypobranchial mass by
the visceral muscles, and produce there merely part of the throat
and neck muscles. Primitively in vertebrates the muscle fibers
extended from myocomma to myocomma and only the fibers
nearest the vertebrae gained an attachment to the axial skeleton.
In fishes the somatic muscles are already sharply divided, by a
horizontal myoseptum or connective tissue plate, into a dorsal
ep axial mass — the definitive back muscles, and a ventral hypaxial
mass — the body wall, the lower portion of the tail musculature-
and the ventral throat muscles. The epaxial muscles are inner
vated by dorsal branches, the hypaxial by ventral branches of
the spinal nerves. In fishes the epaxial muscles are greater in
volume than the hypaxial and serve with the latter to bend the
body from side to side in swimming. In Amphibia, the epaxial
muscles are reduced, and correlated with this, the horizontal
septum together with the transverse processes of the ribs are
pushed to a higher level on the side of the vertebral column.
Less dependence on the epaxial (dorsal) muscles occurs during
locomotion, until in frogs the epaxial muscles serve to bend the
vertebral column dorsally instead of laterally (Fig. 91). The
hypaxial muscles, also, show marked changes in correlation
with terrestrial life. This is far greater in the body wall, which
serves for supporting the viscera and for respiratory movements,
than in the tail, which still functions in locomotion. With the
reduction of their locomotory functions, the hypaxial (ventral)
muscles give rise to a subvertebral system which comes to
underlie the vertebrae and ribs. Before considering the modifica-
tions of the hypaxial (ventral) system in detail, some further
reference may be made to the epaxial musculature, since the

250

THE BIOLOGY OF THE AMPHIBIA

frogs with their short bodies and leaping movements have
molded this epaxial (dorsal) musculature in correlation with their
distinctive habits.

In urodeles the epaxial muscle mass is divided by myocommata

into the same number of seg-
ments as there are vertebrae.
Most of the muscle fibers run
from myocomma to myocomma
as in fish, but these septa show
little of the folding so charac-
teristic of the dorsal muscles of
swift-swimming fish. Proxi-
mally each myocomma makes a
firm attachment to a single
vertebra in adult Amphibia,
although in some larvae the
proximal attachment extends
to several vertebrae, a piscine
condition and one apparently
correlated with the elastic and
poorly jointedvertebral column.
The muscle fibers adjacent to
the vertebrae are more or less
attached to them, forming short
intersegmental bundles. In
the Salientia this deep muscle
formation is carried much
farther, and definitive Mm.
intertransversarii and inter-
neurales between the transverse
processes and the neural arches,
respectively, may be distin-
guished in the more advanced
groups where they have split from the primitive M. dorsalis trunci
mass. Further, a lateral ileolumbaris is present on each side in
frogs of several families. The overlying muscle fibers, while more
or less fused in Ascaphus, become free of these intervertebral
muscles in Discoglossus and in most frogs form a long muscle ex-
tending from head to coccyx, the M. longissimus dorsi. Although
V-shaped myocommata are retained, they make little or no

Fig. 91. — Dorsal body musculature
of Bombina maxima. C.I., Coccygeo-
iliacus; C.S., coccygeo-sacralis, Di-s,
longissimus dorsi, successive segments;
D.M., depressor mandibulae; D.S.,
dorsalis scapulae; I.L., ileolumbaris;
Lot., latissimus dorsi; Pt., pterygoideus;
S., sacral diapophyses; Tern., temporalis.

THE MUSCULAR SYSTEM

251

muscle fibers of frogs have practically given up their original
function of lateral bending but have assumed new functions of
holding up the head in leaping and of bending the body sharply
upward in a so-called " warning" attitude (Chap. XVI).

Although both urodeles and Salientia have very short necks,
many species are capable of bringing the head to a lateral
position nearly at right angles to the main axis of the body.
Such a movement is facilitated by a division of the anterior
part of the M. dor salts trunci into several muscle bundles which

/V B C D

Fig. 92. — A comparison of the ventral body musculature of various Amphibia.
Schematic cross-sections through the middle of the body. A. Triturus, larva.
B. Triturus, adult. C. Salamandra, adult. D. Rana, adult. D.M., back
musculature; O.E., M. obliquus externus abdominis; O.E.P., M. obliquus exter-
nus profundus; O.E.S., M. obliquus externus superficialis; 0.1. , M. obliquus
internus; P.M., M. pectoralis; R., M. rectus abdominis; R.L., rectus lateralis;
R.P., rectus profundus; R.S., rectus superficialis; S.V., subvertebralis; Tr.,
transversus. {After Maurer.)

extend to the skull. In the newt there are three of these mus-
cle heads, an apparent fourth being the temporalis, a visceral
jaw muscle which extends to the neural spine of the first verte-
bra of many urodeles and is especially well developed in the
species of Desmognathus.

The hypaxial musculature of the early urodele larva approaches
the condition in fish. Myocommata are present and the fibers
instead of running longitudinally, as assumed for the primitive
vertebrate, are arranged into two layers of oblique fibers, the
outer running ventroposteriorly and the inner, dorsoanteriorly,
that is, in the opposite direction. These are the Mm. obliquus

252

THE BIOLOGY OF THE AMPHIBIA

externus and internus, while the medioventral fibers which
retain the primitive longitudinal direction form the M. rectus
abdominis. There develops in some aquatic larvae such as
those of the newt a muscle bundle just below the horizontal
septum which appears to be homologous with the M. rectus
lateralis an important swimming muscle of many teleosts (Ver-
sluys, 1927). As the larva develops, the hypaxial muscles
differentiate further from the fish condition until at metamor-
phosis radical changes frequently occur (Fig. 92). The first
change during development is the differentiation of an additional
muscular layer outside the original outer oblique layer and
another inside the original inner oblique layer. Further, the
rectus may also split off an outer layer. In this way four oblique
and two rectus muscles may arise in the mature urodele larva.
The muscles, reading from the outside in, are called M . obliquus
externus superficialis, M. o. e. profundus, M. o. internus, and M.
transversus, also M. rectus superficialis and M. r. profundus
(Maurer, 1892, 1911). At metamorphosis the rectus lateralis
may disappear and the secondary hypaxial muscles increase in
thickness.

Modification of Body Muscles. — The various genera of uro-
deles show differences in the body muscles for which there is
claimed both phylogenetic and functional significance. In the
terrestrial Salamandra there are four muscle layers forming the
body wall of the larva, but the M. o. internus and the M . trans-
versus fuse together during metamorphosis. On the other hand,
in the aquatic Cryptobranchus the Mm. o. e. superficialis and
profundus are fused or possibly never separate, the conditions in
the early larvae being unknown. In the different genera of
urodeles the superficial rectus shows various degrees of freedom
from the profundus and the latter from the primary obliquus
externus and internus of its origin. Failure of the M. rectus
profundus to separate from the latter may be considered a larval
condition retained by the perennibranchs. The condition is,
however, found in a few metamorphosed types such as the newt
(Fig. 921?). A progressive change found developed to various
degrees in the different groups of urodeles is the loss of the myo-
commata in the body muscles. In Amphiuma, for example,
this loss of segmentation occurs in both the M. o. e. superficialis
and the M . transversus. In the case of the former it might be
correlated with the digging habits of the species. The loss of

THE MUSCULAR SYSTEM

253

the myocommata frees the muscle layers from adjacent integu-
ment or muscle and makes possible independent action. There
are, in brief, two tendencies of urodele evolution found in these
body muscles: first, reduction in number of layers; and second,
loss of metameric structure.

In the Salientia these tendencies are carried nearly to comple-
tion. The primary oblique muscles form a single sheet as in
very young but not older urodele larvae (Maurer, 1895). Fur-
ther, this combined obliquus externus and internus is replaced
just before metamorphosis by the secondary M. obliquus externus
superficialis and M. transversus. The M. rectus abdominis
develops in the tadpole as a single muscle and remains un-
divided in the adult frog. The myocommata are not formed
in the first two muscles and only the rectus retains the original
segmentation.

While the reduction of the number of muscles in the body wall
may be traced from the axolotl to the frog, there remains to be
considered what the primitive condition may have been in
Amphibia. Reptiles, although terrestrial, exhibit no reduction
of hypaxial muscle layers. On the contrary, in addition to the
four muscle layers forming the body wall of the newt, they have
two additional layers associated with the ribs. Since the bran-
chiosaur ancestors of frogs and salamanders had short ribs, they
presumably possessed no such development of the hypaxial
muscles as is found in modern reptiles. The reduction of the
primary hypaxial muscles at metamorphosis in the Salientia
would apparently be correlated with the absence of the ribs rather
than with the assumption of terrestrial life. We may conclude
that four layers of muscle formed the body wall of the primitive
amphibian larva, and that the two primary or central layers
were reduced in correlation with the degeneration of the ribs
in the metamorphosed adult.

The hypaxial muscles of the tail retain the primitive metam-
erism, and the muscle fibers run longitudinally between the
myocommata. In the pelvic region two muscle bundles gain an
insertion on the hind limb of each side and assume important
functions in walking. Many urodeles, both aquatic and terres-
trial forms, are able to use their tails as prehensile organs, but
as the tip is merely moved to the side, no fundamental changes of
musculature, such as is found in the chameleon's tail, for example,
are made in this appendage.

254

THE BIOLOGY OF THE AMPHIBIA

Ventral Throat Musculature. — The rectus abdominis is contin-
ued forward into the throat region by the sternohyoideus or
abdominohyoideus of urodeles. The latter muscle is part of the
hypaxial system, but its union with the red us is apparently second-
ary, since the labyrinthodonts had a better developed pectoral
girdle than modern urodeles, and this would have separated the
two muscles (Miner, 1925). The condition in Salientia where

Fig*. 93. — Dissection of the hyobranchial muscles of the adult Eurycea bisline-
ata, dorsal view. The dorsal surface of the tongue has been partly removed
and the posterior edge entirely so, to show underlying muscles. A.H., abdomino-
hyoideus; A.H.S., abdominohyoideus ventral slip; C.B. i_2, ceratobranchial I
and II; C.H., ceratohyal; C.H.I., ceratohyoideus internus; D.A., depressores
arcuum; G.H.L., geniohyoideus lateralis; H., horn of copula; H.G., hyoglossus;
L., lingual cartilage; O.T., os thyreoideum; S.P., suprapeduncularis. (After
Smith.)

the muscles are separate, although sometimes overlapping, is
more primitive. The sternohyoid is continued to the lower
jaw by the same tongue muscles in both frogs and urodeles.
The geniohyoideus extends from hyoid to the anterior margin
of the lower jaw, while a median bundle of muscle fibers extends
to the floor of the mouth and forms the bulk of the superficial
tongue muscles (Fig. 93). The detailed arrangement of these
muscles varies with the group of Amphibia considered (Gaupp,
1896; Driiner, 1902, 1904), and in the perennibranch urodeles the

THE MUSCULAR SYSTEM

255

conditions may be more larval than primitive. In some urodeles
and frogs the lateral portion of the sternohyoideus may form a
distinct omohyoideus as in higher vertebrates.

Forelimb Muscles. — The forelimbs of the earliest tetra-
pods were held more or less at right angles to the body and the

Fig. 94. — Ventral body muscles of Liopelma showing the cartilaginous abdomi-
nal ribs which occur in this primitive frog. A.R., abdominal ribs; C.B.B.,
coracobrachial brevis; C.B.L., coracobrachialis longus; C.R.P., coracoradialis
proprius; D., deltoideus; Gl., lymphoidal gland, P.Abd., pectoralis abdominalis;
P.St., pectoralis sternalis; S.S., supracoracoideus.

sharply bent forearms supported the weight. The humerus was
advanced and the forearm extended, or the humerus brought
posteriorly and the forearm flexed. The musculature of the
forelimb, as far as it may be judged by the form of the limb and
girdle, consisted of a ventrolateral and a dorsomedial group of
muscles, which Romer (1924) has homologized with the muscle
masses found one on either side of the anterior fins of fish.

256

THE BIOLOGY OF THE AMPHIBIA

The hind limbs also were held astraddle when at rest, and a dorsal
and a ventral group of muscles could be inferred in the early
tetrapods. The limb muscles have presumably split from the
hypaxial musculature during phylogeny, but modern Amphibia
show no evidence of such origin in their ontogeny (Lewis,
1910; Rylkoff, 1924). The musculature of fore- and hind limbs
was not alike in detail even in the most primitive tetrapods.
Such a difference was correlated with the different structure
of the pectoral as compared with the pelvic girdle inherited from

Fig. 95. — Dissection of the arm and shoulder musculature of Megalobatrachus.
anc.lat., M. anconeus lateralis; anc.scap., M. anconeus scapularis; bri., M.
brachialis inferior; cbl., M. coracobrachial longus; delt.scap., M. deltoides
scapularis-dorsalis scapulae; ext. carp. rad., M. extensor carpi radialis; ext.carp.uln.,
M. extensor carpi ulnaris; ext. dig. long., M. extensor digitorum longus; lev. scap.,
M. levator scapulae; Id., M. latissimus dorsi; p., M. pectoralis; procor.hum., M.
procoracohumeralis; serr.pro., M. serratus profundus; spc, M. supracoracoideus;
sup. long., M. supinator longus; trap., M. trapezius. (After Miner.)

fish. Further, the forelimbs were early used to raise the body,
while the hind limbs pushed it forward. In correlation with this
functional difference, the elbow joint formed in the forelimbs
tended to be directed backward like that of modern Amphibia,
while the knee joint gave a better purchase when directed
forward. This functional difference, continued in phylogeny,
affected the distal segments least and a great similarity may
still be found in the distal muscles of the fore- and hind limbs of
modern salamanders such as Necturus (Wilder, 1908). Although
the pelvic girdle very early in the history of the first tetrapods
gained a firm attachment to the vertebral column, the pectoral

THE MUSCULAR SYSTEM

257

girdle, apparently in correlation with the requirements of respira-
tion, did not succeed in the amphibian series in securing a similar
support. Hence, the forelimb muscles in Amphibia spread
dorsally and ventrally over the body, the pectoralis group of each
side meeting ventrally in the midline in many species (Fig. 94),
while in some aquatic and burrowing types which use their fore-
limbs to a considerable extent, one of the dorsal muscles (M.
latissimus dor si) came to cover a considerable part of the back.
Although some hypaxial muscles attach to the pelvis and femur,
these are tail muscles which utilize the swing of the caudal
appendage to pull the legs posteriorly, and they may be sharply
contrasted to the several powerful hypaxial muscles which
extend from the ribs, transverse processes or skull, to give support
to the pectoral girdle. The chief muscle masses which originally
attached to the cleithrum and scapula of labyrinthodonts
extend mainly to the suprascapula of modern Amphibia, a
levator group forming an anterior mass and a serratus group form-
ing a posterior one (Fig. 95). The musculatures of the fore-
and hind limbs do agree, however, in being formed of short,
deep muscles extending over one limb joint and of long, more
superficially placed muscles reaching over two or more limb
segments.

Comparison of Frog and Salamander. — A detailed comparison
of the limb muscles of the various groups of Amphibia lies
beyond the scope of the present discussion. Still, the proximal
limb muscles of common frogs and salamanders seem at first
glance so very different in the two groups that the similarity of
plan may be emphasized here. If the skin from the chest and
upper arm of such a primitive frog as Ascaphus or Liopelma
be peeled back and the muscles compared with those from the
same region in Megalobatrachus or other primitive urodele, a
remarkable resemblance will be noted. The urodeles have lost
the dermal shoulder girdle, and the long slip of muscle found in
the frogs, running from the ventral surface of the head of the
humerus to the mesial end of the clavicle and called by Anthony
and Vallois (1914) episterno-cleido-humeralis longus, has disap-
peared unless it is represented by a muscle carried forward on the
anteriorly directed procoracoid cartilage of salamanders. Except
for this difference, the number and arrangement of the muscles
covering the ventral surface of the pectoral girdle of frogs and
urodeles are the same. Beginning at the anterior end there is a

258

THE BIOLOGY OF THE AMPHIBIA

supracoracoideus covering coracoradialis proprius and inserting
on the ventral process of the humerus. The latter deep-lying
muscle is continued in all frogs and many salamanders as a tendon
hidden among the muscles of the upper arm to the radius, which
accounts for its name. Superficially covering the chest a broad
pectoralis muscle lies immediately caudal to the supracoracoideus
and with the latter covers two coracobrachialis muscles which
extend between humerus and coracoid (Fig. 94). All of these
muscles belong to the ventrolateral muscle mass in the earliest
tetrapods and in their fish ancestors. The muscles on the flexor
aspect of the forearm and hand of Amphibia also are part of this
mass. It would hardly be inferred from a superficial examination
of modern Amphibia that the dorsalis scapulae, originating on the
suprascapula and inserting on the ventral process of the humerus,
also belonged to this ventrolateral group. In the earliest
Amphibia the cleithrum formed the anterior border of the cora-
coscapula, and the dorsalis scapulae was part of a deltoideus
mass which had a broad seat of origin along this dermal element
(Miner, 1925). With the reduction of the cleithrum in frogs
the deltoideus was split into two or more masses, one of which
formed the dorsalis scapulae, another the episterno-cleido-
humeralis longus (= deltoides clavicularis) of frogs, some fibers
remaining in the original central position marked by the acromion
process and forming the acromio-cleido-episterno-humeralis of
Anthony and Vallois. In urodeles the cleithrum has been lost
entirely and the only evidence of the former continuity of the
dorsalis scapulae and the procoracohumeralis is their common
innervation.

The pectoral musculature has undergone some modification in
the phylogeny of both frogs and salamanders. All Pelobatidae,
as far as known, have the episterno-cleido-humeralis longus fused
with the supracoracoideus, and the caudal part of the latter muscle
retains the primitiveness of Discoglossidae in remaining a single
muscle instead of splitting off a supracoracoideus profundus as in
many Bufonidae (Noble, 1926). The pectoral musculature of
Rana is highly specialized but not so much so as in the case of
many Brevicipitidae which have lost the clavicle and procoracoid
and piled the pectoral muscles close together. The pectoralis is
usually split into a sternal and an abdominal portion in
Salientia. The latter may extend to the thighs in some species
of frogs.

PRIVATE LIBRARY OF
ALBERT G. SMITH

THE MUSCULAR SYSTEM 259

The muscles of the dorsomedial group show far less specialization
than those of the ventrolateral group, and not only are frogs and
salamanders alike in regard to the general form and arrangement
of the several muscles comprising this series, but the homologous
muscles in reptiles and mammals may be recognized from their
positions relative to the bones and to one another. Beginning
at the proximal end of the series a latissimus dorsi is found in
both frog and salamander originating from a broad base on the
dorsal fascia immediately caudal to the dor salts scapulae and
narrowing to its insertion on the head of the humerus or its
capsules. Hidden from view by more laterally placed muscles,
the subcoracoscapularis is the second muscle of the series. It
runs from the posterior margin of scapula and coracoid to the
medial process of the humerus. Its head of origin is thrust
between two of the heads of the anconeus or triceps, the third
muscle of the series to consider. The latter is the large muscle
covering the dorsal side of the upper arm. It originates from
four heads on the scapula, coracoid, and humerus which merge
into a single muscle inserting on the ulna. Obviously this is the
chief muscle for extending the lower arm. The more distal
muscles on the extensor surface of forearm and hand are the
final part of the dorsomedial series. A part of the lower-arm
muscles arises from the humerus, the extensor muscles from the
ectepicondyle. These work in opposition to the flexor muscles
which arise from the entepicondyle and cover the ventral surface
of the arm and hand. In primitive tetrapods with their heavy
bodies and broad trackways these distal condyles of the humerus
were greatly expanded. The muscles serving for the movement
of hand and fingers have been considered by Gaupp, 1896;
Ribbing, 1907; Miner, 1925; and others. In general, during both
ontogeny and phylogeny there is a reduction of the short muscles
of this region and their functional replacement by the longer
muscles. The same maintains for the evolution of the muscles of
the feet.

Hind Limb Musculature. — The musculature of the hind limb
may be considered briefly. The pelvis of frogs is short and
narrow, that of urodeles longer and flatter. This has a marked
effect upon the arrangement of the proximal muscles especially
as viewed from the ventral surface after removing the skin.
Nevertheless, when the musculatures of primitive frogs and
urodeles are compared, a general agreement of plan will be recog-

260 THE BIOLOGY OF THE AMPHIBIA

nized which may be taken as evidence that the two groups arose
from ancestors having a common type of musculature (Fig. 96).
It is this common plan which must be compared with the hind-
limb musculature of higher vertebrates in deducing homologies;
the mammalian names given to the muscles of the specialized
Rana are for the most part erroneous (Noble, 1922, Table 1).

If we compare the muscles on the ventral surface of the thigh
of such primitive genera as Ascaphus and Rhyacotriton, a con-
siderable resemblance will be noted (Fig. 96), the chief differences
being that some of the same muscles which are dorsally arranged
in the salamander cover the anterior portion of the thigh of the
frog and that the two muscles extending between thigh and tail
of the salamander are not visible, for they have been carried
dorsally by the reduction of the tail. Anteriorly on the ventral
surface of the thigh of salamanders is a pubotibialis overlying a
deep puboischiofemoralis internus. Their innervations as well
as their origins and insertions show that these muscles are
homologous with the so-called ventral head of the adductor
magnus and the deep-lying pectineus of frogs, respectively. Two
large muscles caudal to the pubotibialis and forming the bulk of
the muscles covering the ventral surface of the thigh, the pubois-
chiofemoralis externus and the puboischiotibialis, are homologous
to the muscles having a similar position in the frog, the first to
the dorsal head of the adductor magnus and the second to a single
muscle which represents the combined sartorius and semitendino-
sus of higher Salientia. Some reference is made to these muscles,
for the changes which take place in the ventral thigh musculature
are often diagnostic of higher groups (Noble, 1922, 1926). The
most posterior thigh muscle in Rhyacotriton, the ischioflexorius,
appears to be a dorsal muscle and in the frogs it is represented
by the semimembranosus, a large muscle on the dorsal side of the
femur. A part of this ischioflexorius, however, forms a distinct
muscle or pair of them on the posterior margin of the thigh in
the Salientia. This is the gracilis major and its separate slip,
the gracilis minor. Obviously the urodele names, expressing
as they do the origins and insertions of each muscle, are more
adequate than the names in common use for the frog muscles.
The literature available concerning the muscles of frogs employs
for the most part the latter names, and hence both have been
indicated in the present brief comparison.

262

THE BIOLOGY OF THE AMPHIBIA

The muscles on the dorsal surface of the thigh in Rhyacotriton
and Ascaphus (Figs. 96A and B) show even a closer resemblance
than those of the ventral surfaces do. There is the same number
of elements and these have nearly the same mutual relationships.
The ilium is carried far forward in frogs and the puboischiofemor-
alis internus forming the anterior margin of the thigh in Rhyaco-
triton is pulled out into an iliacus externus. The iliotibialis
has shortened in Ascaphus and it remains so in all higher frogs
where it is called the tensor fasciae latae. The two ' ' tail- wagging ' '
muscles, caudalipubofemoralis and caudalipuboischiotibialis, are
both present, although very small in the frog and extending to
the coccyx. The first masquerades under the name of pyriformis
in the frog, but as this muscle is apparently homologous with the
pyriformis of mammals it may well be substituted for the caudali-
pubofemoralis of salamanders as well. The remaining muscles
on the dorsal surfaces of the two thighs offer no difficulty. The
ilioextensorius is obviously homologous with the combined cruralis
and glutaeus, which are, however, very much more powerful in
frog than in salamander. The iliofibularis is homologous with a
muscle of the same name in frogs. The ischioflexorius has already
been stated to be the homologous equivalent of the combined
semimembranosus and gracilis. A small part of the deep-lying
iliofemoralis shows on the dorsal surface of the thigh of Rhyaco-
triton, and this is homologous with a muscle of the same name
covered by the iliofibularis in the frog. In mammals the ilio-
femoralis becomes the important glutaeus group which draws the
chief trochanter of the femur forward and hence the leg back-
ward in running. The other deep muscles of the frog's thigh
need not be mentioned, although they are homologous with
muscles in the urodele and have undergone certain changes in the
evolution of the various groups. Homology is determined by
the origin and insertion of a muscle, its relation to adjacent
muscles, and its innervation in a natural series of forms. Func-
tion is no criterion of homology even in related groups. Thus,
the ilioextensorius carries the knee dorsally in salamanders on
contraction, while the homologous cruralis and glutaeus in frogs
bring the knee forward and extend the lower leg. If the flexors
on the back of the thigh are tense in the frog, however, the
contraction of the same muscle causes a flexion of the leg. The
action of any muscle when working alone is different from that
produced by several acting together.

THE MUSCULAR SYSTEM

263

Visceral Muscles. — In the discussion of the forelimb muscula-
ture no reference was made to a conspicuous muscle, the trapezius,
arising from skull or dorsal fascia and inserting on the scapula.
This is one of the visceral muscles which forced the epaxial mus-
cles dorsally, the hypaxial, ventrally, in reaching their super-
ficial position on the side of the neck. The other visceral muscles
include the jaw, hyoid, and gill muscles. In fact, with the excep-
tion of the tongue, eye, and some medioventral throat muscles,
all the musculature of the head is visceral. In the larvae of
urodeles and frogs there are a superficial constrictor of the bran-
chial arches and a deep-lying set of levators, marginales, and
other slips controlling the movements of the gill arches. A similar
superficial constrictor and a deeper series of short muscles
derived from it occur in fishes, some of which possess also a
trapezius inserting on the shoulder girdle. At metamorphosis
with the disappearance of the gill arches, all of these visceral
muscles dwindle away except the trapezius, which retains its
original position relative to the pectoral girdle. In the frog,
however, the series of levatores arcuum are retained as a group of
petrohyoidei extending from skull to hyoid plate and serving to
raise the hyoid apparatus and carry it forward.

The hyoid arch primitively in fish is surrounded by a con-
strictor belonging to the same series as the more posterior con-
strictors. In Amphibia this constrictor is divided by the hyoid
into a pair of dorsal muscles which develop as the depressor
mandibulae or mouth-opening muscles, while the ventral portions
of the same pair of muscles join in the midline to form a muscle
which is more or less distinct in both urodeles and frogs. These
constrictors of the hyoid are innervated by the facialis nerve,
while the more posterior visceral muscles are supplied by the
glossopharyngeus and vagus. The depressor mandibulae may arise
entirely from the skull or have a second, more posterior part in
many Salientia arising from the suprascapula.

The constrictors of the jaws are innervated by the trigeminus
and hence are readily distinguishable from the hyoid constrictors
which may encroach upon their territory ventrally. The jaw
constrictors were split early in the phylogeny of the vertebrates
into three pairs of muscles, of which the adductor mandibulae is
the most important. These adductors are divided into two or
more parts in Amphibia (Lubosch, 1914). The temporalis inserts
on the coronoid process of the lower jaw and extends back to a

264

THE BIOLOGY OF THE AMPHIBIA

point of origin on the first cervical vertebra of many urodeles
(Dubecq, 1925) but mainly to the cranial roof in frogs. The
pterygoideus extends from the pterygoid or side of the brain case
and inserts on the lower jaw. In the Salientia two slips of the
temporalis make separate attachment to the squamosal or quad-
ratojugal and are called "masseters" in allusion to a possible
homology with the masseters of mammals. The changes in
shape and distribution of these adductor mandibulae muscles are
closely correlated with the shape of the skull.

The ventral segments of the constrictors of the jaws unite to
form the submaxillary or superficial throat muscles of Amphibia.
An anterior portion is differentiated in frogs to raise the men-
to-Meckelian bones at the anterior angle of the lower jaw and is
called the submentalis. The various natural groups of Amphibia
often show differences in their visceral musculature (Druner,
1902, 1904; Smith, 1920; Edgeworth, 1923) of systematic value.
The phylogenetic change in the hyoid and other bony structures of
Amphibia is closely correlated with changes in their musculature.

References

Anthony R., and H. Vallois, 1914: Sur la signification des elements ven-
traux de la ceinture scapulaire chez les batraciens, Bibl. Anat., XXIV,
218-276.

Detwiler, S., 1920: Experiments on the transplantation of limbs in Amblys-

toma; The formation of nerve plexuses and the function of limbs, Jour.

Exp. Zool, XXXI, 117-169.
Druner, L., 1902: Studien zur Anatomie der Zungenbein-Kiemenbogen

und Kehlkopfmuskeln der Urodelen, I. Teil, Zool. Jahrb. Anat. Abt.,

XV, 435-622, pis. 25-31.
, 1904: Studien zur Anatomie der Zungenbein-Kiemenbogen und

Kehlkopfmuskeln der Urodelen, II Teil, Zool. Jahrb. Anat. Abt.,

XIX, 361-690, 12 pis.
Dubecq, J., 1925: Constitution du muscle temporal chez les amphibiens

urodeles: signification morphologique de ce muscle, Compt. rend. Soc.

Biol, XCIII, 1523.
Edgeworth, F. H., 1923: On the larval hyobranchial skeleton and mus-
culature of Cryptobranchus, Menopoma and Ellipsoglossa, Jour.

Anat., LVII, 97-105.
Gaupp, E., 1896: "Ecker's and Wiedersheim's Anatomie des Frosches,"

Braunschweig.

Lewis, Warren H., 1910: The relation of the myotomes to the ventro-
lateral musculature and to the anterior limbs in Amblystoma, Anat.
Rec, IV, 183-190.

Lubosch, W., 1914: Vergleichende Anatomie der Kaumuskeln der Wirbel-
tiere, in fiinf Teilen, I Teil: Die Kaumuskeln der Amphibien, Jena.
Zeitschr., LIII, 51-188, 5 pis.

THE MUSCULAR SYSTEM

265

Mangold, O., 1929: Das Determinationsproblem; II. Die paarigen Extremi-
taten der Wirbeltiere in der Entwicklung, Erg. Biol., V, 290-404.

Maurer, F., 1892: Der Aufbau und die Entwicklung der ventralen Rumpf-
muskulatur bei den urodelen Amphibien und deren Beziehungen zu
den gleichen Muskeln der Selachier und Teleostier, Morph. Jahrb.,
XVIII, 76-179.

, 1895: Die ventrale Rumpfmuskulatur der anuren Amphibien,

Morph. Jahrb., XXII, 225-263.
, 1911: Die ventrale Rumpfmuskulatur von Menobranchus, Meno-

poma und Amphiuma, verglichen mit den gleichen Muskeln anderer

Urodelen, Jena. Zeitschr., XL VII, 1-40.
Miner, Roy Waldo, 1925: The pectoral limb of Eryops and other primitive

tetrapods, Bull. Amer. Mus. Nat. Hist, LI, 145-312.
Noble, G. K., 1922: The phylogeny of the Salientia; I. The osteology and

the thigh musculature; their bearing on classification and phylogeny,

Bull. Amer. Mus. Nat. Hist., XLVI, 1-87, pis. 1-XXIII.
, 1926: An analysis of the remarkable cases of distribution among

the Amphibia, with descriptions of new genera, Amer. Mus. Novit.,

No. 212.

Ribbing, L., 1907: Die distale Armmuskulatur der Amphibien, Reptilien

und Saugetiere, Zool. Jahrb., XXIII, 587-683, 2 Taf.
Romer, A. S., 1924: Pectoral limb musculature and shoulder-girdle structure

in fish and tetrapods, Anat. Rec., XXVII, 119-143.
Rylkoff, Helene (Woronesch), 1924: Die Entwicklung der Schulter-

muskeln bei urodelen Amphibien, Zeitschr. Wiss. Zool., CXXII, 116-171.
Smith, Louise, 1920: The hyobranchial apparatus of Spelerpes bislineatus,

Jour. Morph., XXXIII, 527-583.
Versluys, J. J., E. W. Ihle, and P. N. van Kampen, 1927: " Vergleichende

Anatomie der Wirbeltiere," Berlin.
Wilder, H. H., 1908: The limb muscles of Necturus, and their bearing upon

the question of limb homology, (Amer. Soc. Zool.), Science, n. s., XXVII,

493-494.

CHAPTER XII

THE UROGENITAL SYSTEM

The excretory and reproductive systems, although originally
separate as in most invertebrates, are so closely associated in
vertebrates, including Amphibia, that they may be considered
together. The waste products of metabolism must be removed
from the tissues of the body if the animal is to live. They are
swept from the tissues by the blood and especially by the lymph,
then carried to those parts of the body where they may be
discharged. Lungs and skin both throw off carbon dioxide and
water as metabolic products. The skin may also dispose of some
salts and possibly some urea. The latter, (NH2)2CO, is a white,
crystalline compound, soluble in water. It is a product of protein
metabolism and is formed in most vertebrates in the liver by the
conversion of nitrogen from protein combustion. From the
liver the urea passes into the blood and is eventually eliminated
chiefly by the kidneys. Foreign substances in the blood, both
organic and inorganic, may also be removed by the kidneys.
In birds and terrestrial reptiles nitrogen is excreted largely as
uric acid, in a semi-solid form. This is apparently an adaptation
toward economy of water and seems to have arisen under arid
environmental conditions such as have been assumed to have
confronted the early reptiles. Although the formation of urea
is believed to be restricted to the liver, Gottschalk and Nonenn-
bruch (1923) found that the urea content of liverless frogs
remained the same as that of normal frogs after the injection of
amino-acids. This has led Buddenbrock (1928) to suggest that
the method of forming urea in the blood directly from ammonia
may be the more primitive one, perhaps characteristic of all
Anamnia.

Urogenital Organs. — The kidneys in vertebrates may have been
primitively a pair of narrow elongate bodies extending the
whole length of the body cavity, a condition which is approached
among Amphibia by Ascaphus and the caecilians. These kidneys
were formed by a series of segmentally arranged tubules resem-

266

THE UROGENITAL SYSTEM

267

bling roughly the sweat glands of mammals, and, like them, they
are excretory organs. The anterior part of such a kidney rudi-
ment theoretically, if not actually present, develops in most lower
vertebrates into a functional organ, the pronephros, before the
posterior section, the mesonephros, differentiates. The former
is the typical kidney of the young larvae, and in forms such as
Eleutherodactylus, which hatch from the capsules as metamor-
phosed individuals, it shows a very early degeneration. In other
Amphibia it functions up to the time of independent feeding or a
little later.

Both pronephros and mesonephros arise from the mesomere,
a portion of the mesoderm lying between the myotomes and the
non-segmented lateral plates of the embryo (Fig. 97). In uro-
deles two or three or at most four segments (Megalobatrachus,

FiGo 97. — Diagram of the development of the pronephric canal. Gl., glomeru-
lus; L.PL, lateral plate; P.C., pronephric canal; Mes., mesomere; My., myotome,
N.S., nephrostome; N.T., neural tube. {After Felix.)

Mibayashi, 1928) of this mesomere give risg^€© tubules, usually
one to each segment. These collective^?6j^n>%ne pronephros.
The tubules open proximally into tj^^dj^cllvity in the form of
nephrostomes, while distally tM?'en^s%end caudally and fuse
to form a common pronep1?nc^i^S;1b. This grows posteriorly
immediately under the ectoderm and finally fuses with the cloaca.
In Salientia, as in most urodeles, only two or three tubules enter
into the formation of the pronephros, while in caecilians the num-
ber involved is from 10 to 13. In the wall of the body cavity of
the larva, adjacent to the proximal openings or nephrostomes
of the pronephric tubules, a series of branches from the dorsal
aorta push out a fold of the peritoneum to form a sinus, the
glomus, which serves as the arterial blood supply. In some
forms, at least, these blood vessels are originally metamerically
laid down as in the case of the tubules. The blood is carried
away by the postcardinal veins which form a plexus about the
tubules.

268

THE BIOLOGY OF THE AMPHIBIA

The mesonephric tubules arise in the same way as do those of
the pronephros, but in growing distally they frequently fuse
with the common pronephric duct. Their proximal ends form
a series of nephrostomes or openings into the body cavity similar
to those of the pronephros. Vessels from the dorsal aorta push
in between the tubules to form a vascular pocket or glomerulus
in the wall of each tubule instead of uniting to produce a plexus
within the body cavity as in the case of the pronephros. The
mesonephric tubules arise in a strictly metameric order in cae-
cilians, Amphiuma, and some others, but in most Salientia and
urodeles secondary tubules early develop and obscure this
arrangement. In urodeles the secondary tubules are derived by
budding from the primary ones after they have attained a func-
tional state. In some Salientia such as Rana temporaria the
whole process of differentiation is apparently speeded up, for the
secondary tubules arise independently from the blastema (Gray,
1930). The collecting tubules which form outlets for the second-
ary tubules arise as short, straight ducts with only abortive
enlargements at their proximal ends as evidence of their phylo-
genetic origin from primary tubules. The mass of mesonephric
tubules forms an elongate organ on the dorsal surface of the
body cavity. In Rana this kidney may include over 5,000
glomeruli (Hayman, 1928), although 2,000 is the average. In
perennibranchs and derotremes the mesonephric kidneys project
into the body cavity and are surrounded on both sides by
peritoneum.

Each tubule (Fig. 98) in the mature kidney, or mesonephros,
of both urodeles and frogs exhibits typically certain structurally
different parts which may be homologized with similar parts of
the tubules of the mammalian kidney, a metanephros. The
nephrostomes on the ventral surface of the kidney open into a
short ciliated neck which connects with a similarly ciliated tubule
extending to an enlarged chamber, the glomerular capsule.
One part of this chamber is invaginated by a rete of arterioles,
the glomerulus, which with its capsule is called a " renal cor-
puscle." The first segment of the tubule which arises from the
capsule is ciliated as stated above. Distal to this first segment,
the tubule widens out into a long convoluted part lined with
cells having a glandular appearance. This is the proximal
convoluted portion of the tubule. It runs dorsally in most
Amphibia, usually to the upper portion of the kidney where it

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269

joins a second ciliated part. This part is sometimes designated
as the narrow segment of the tubule, although it may be as wide
as all the other segments except the proximal ciliated one. It
corresponds in position to Henle's loop of the mammalian kidney,
and although it may extend ventrally again it has neither the
great length nor the characteristic form of this important part
of the metanephric tubule of the mammalian kidney. There
follows on this segment the fourth or distal convoluted portion
of the tubule. It is joined by a short junctional segment with

Tb. J. p.

Fig. 98. — Diagrammatic section of the kidney of Necturus maculosas to show
the form of a typical tubule and its relation to the blood supply. A.D., dorsal
aorta; A.R., renal artery; Cap., capillary; C.N., ciliated neck; Ms., mesentery;
Neph., nephrostome; R.C., renal (Malpighian) corpuscle; R.V., renal portal
vein; Tb.Ex., outer tubule; Tb.J.P., junctional part of renal tubule; Tb.N.P.,
narrow part of renal tubule; Tb.Sec.P., proximal convoluted part of renal
tubule (secretory part in pelvic kidney) ; Tb.Str.P., distal convoluted part of
renal tubule (.striated part in pelvic kidney); V.A., afferent renal vein; V.E.,
efferent renal vein; V.P., vena cava posterior; W.D., Wolffian duct. (After
Chase.)

a connecting tubule which in some frogs extends transversely
across the kidney to make an outlet to the Wolffian duct. These
five parts of the tubule may be seen in Fig. 98.

Many tubules of both urodele and frog kidney lack a neph-
rostome and hence have given up all direct connection with the
coelom. In higher vertebrates, those with a metanephric
kidney, nephrostomes are given up entirely. One modification
of the nephrostome is found only in the Salientia. In many,
but not all, of these the nephrostomal segment of the tubule
joins with nephric veins (Sweet, 1908). Originally the nephro-
stomes discharged into the tubules waste fluids secreted through

270

THE BIOLOGY OF THE AMPHIBIA

the walls of the peritoneum, but within the Amphibia apparently
with the increasing use of the peritoneal cavity as a lymphatic
chamber these same nephrostomes became conduits for circula-
tory fluids. This offers a good example of structures assuming
totally new functions during phylogeny without changing to
any great extent their original character. It may be further
noted that in Rana temporaria, at least (Gray, 1930), the nephros-
tomal funnels arise independently of the tubules, and hence the
frog shows in its development no evidence of the ancient use of
these structures as essential parts of the excretory system.

Function of the Kidney. — The structural differences between
the kidney tubules of amphibians and those of mammals are
closely correlated with important functional differences. The
mammalian urine is always hypertonic to the blood, i.e., possesses
a higher percentage of solids and accordingly a higher osmotic
pressure. On the other hand, amphibian urine is usually hypo-
tonic to the blood or at least never exceeds it in concentration.
This difference is apparently correlated with the absence of a
typical Henle's loop in the amphibian tubules. Through the
thin membrane covering each glomerulus, there apparently
filters out into the glomerular capsule a fluid which is essentially
blood plasma devoid of its proteins and lipins (Walker, 1930).
The tubules show a selective function in reabsorbing useful
substances especially sodium chloride and glucose and in trans-
mitting them back to the blood stream (Liang, 1929). Dyes have
been frequently injected into the vascular system of frogs with a
view to demonstrating the part of the tubule which eliminates
such foreign substances. It appears that the glomerulus may
eliminate certain dyes and the tubule others (Kuki, 1929).
Bensley and Steen (1928) found by the use of dyes that the distal
convoluted segment of the frog's renal tubule had resorptive
functions, while the proximal section, although taking up the
dye from the blood, excreted it into the tubule lumen in a more
dilute solution. According to these authors, this process of
secretion is present even when there is no circulation in the
renal corpuscles. Bieter and Hirschf elder (1929), on the other
hand, have stressed the rapidity with which dye may be elimi-
nated by the glomeruli as contrasted with the slower elimination
by the tubule. In brief, the tubule plays a most important role
in reabsorption, while the glomerulus, with its thin cover of
cells, may be looked upon as a mechanism for flushing the tubule.

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271

In salt-water fish and reptiles which must conserve their water,
the glomerulus may be poorly developed or even, as in some of
the former, absent entirely.

In spite of the dilute character of frogs' urine, certain of its
constituents are very much more concentrated than in either
blood or capsular fluid. This has been shown to be the case for
urea (Przylecki, 1922), where the concentration may be as great
as seventy-four times (Crane, 1927). In comparison with
mammalian urine, however, phosphates are far less efficiently
concentrated in the amphibian kidney, and chlorides and
bicarbonates not at all (Crane, 1927). Crane suggests that the
concentration of urea is probably due to a selective secretory
function of the tubules, and this author points out that this may
be a primitive mechanism which is lost higher in the evolutionary
scale. Throughout the vertebrate series the glomerulus remains
as the primary outlet for water.

Frogs and toads excrete proportionately much more urine per
day at ordinary temperature than man. While man excretes
about one-fiftieth of his weight per day, the frog excretes about
one-third (Adolph, 1927). Like most essential processes in
Amphibia, the rate of excretion is dependent on environmental
temperature. During the winter, kidney function is almost
entirely suspended. This is apparently not due, however,
to the slowing down uniformly of all the processes of excretion.
Oliver and Eshref (1929) have shown that there is an increase in
resorptive functions of the tubules during the winter months.
In Rana pipiens an increase in temperature of 10°C. increases the
rate of water passage through the skin 2.3 times (Adolph, 1930).
At any one temperature the water is absorbed through the skin
at a rather constant rate (Adolph, 1927) and does not vary with
the area of skin exposed. The water is excreted by the kidneys
at the same rate and hence the concentration of body fluids
does not change essentially. The frog thus regulates its fluid
content at the point of output and not at the point of intake.
The blood pressure has an important control over the amount of
urine eliminated, since the blood plasma apparently passes
through the glomeruli by filtration, not by secretion. In
salamanders the destruction of one kidney, either mesonephros
or pronephros (Howland, 1920), results in a compensatory
hypertrophy of the kidney of the opposite side. It would seem
that in this case the amount of water absorbed remained the

272

THE BIOLOGY OF THE AMPHIBIA

same as before the operation and that the one remaining kidney
grew to do the work of two.

In brief, the work of the kidney is not purely excretory, that is,
the elimination of waste products of metabolism. The kidney
has regulatory functions as well. By allowing the passage of
certain substances to the exterior, and in the retention of others,
the kidney is of the greatest importance in maintaining the
characteristic constancy in composition of the body fluids.
Amphibia are continually absorbing water through their skin,
and, further, they take less sodium chloride in their food than
mammals. Hence, the materials eliminated are different in the
two groups. In mammals water is saved and the salts excreted,
while in Amphibia the reverse maintains to a large degree.
Further, with the less efficient regulatory mechanism of the
amphibian kidney, the bladder (to be discussed below) functions
not merely as a receptacle for urine. Since the bladder is
permeable to water, there is an absorption by the tissues of water
from the bladder under conditions of dehydration until the
osmotic equilibrium with the blood is again attained (Steen,
1929).

One modification of the amphibian kidney requires further
mention, for it has apparently considerable phylogenetic signifi-
cance. The mesonephric tubules of caecilians exhibit a type of
modification not found in other Amphibia but one which was
taken up and elaborated by the more advanced vertebrates.
While in some Salientia and Caudata the collecting ducts of the
mesonephros are primary tubules which usually extend to
the common pronephric duct to gain exit to the outside, in the
caecilians the posterior part of this duct sends out branches to
the tubules of the kidney before they grow out. In higher
vertebrates these ureters are reduced in number until in some
mammals only a single one is formed. Caecilians thus show the
first step in the origin of the true ureter of higher vertebrates.

Reproductive System. — The ducts of the kidneys are modified
in Amphibia chiefly in correlation with the different methods
of transferring the sexual products to the outside. The common
pronephric duct splits in sharks to give rise to the Mullerian duct
or tube for the passage of eggs to the cloaca, while the remainder,
now called the " Wolffian duct," retains its original function
of a discharge canal for the mesonephros. The Mullerian duct
arises partly from the pronephric duct in Ambystoma but in

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273

frogs and toads has a wholly independent origin from a fusion
and backward growth of two or more evaginations, which
although appearing later than the pronephric tubules seem to be
homologous with them. Hall (1904) has suggested that these
evaginations, which lie ventral to the pronephric nephrostomes,
originally possessed a secretory function which was given up
when they became specialized to subserve a sexual function.
The Mullerian duct develops in both sexes of most Amphibia
but grows to a functional condition only under the influence
of the ovary (Christensen, 1929). The Mullerian ducts usually
open separately into the cloaca in most Amphibia, but in Bufo
and Alytes they may unite just anteriorly to the cloaca, while in
Nectophrynoides the chamber resulting from the fusion produces
a bicornuate uterus in which the young develop.

The spermatozoa gain exit to the outside by way of the Wolffian
duct. A series of genital cords which grow out from the tissues
of the kidney to the developing testis form, at a later stage, a
series of fine ducts to serve as a passageway from the testis to
the mesonephros. The net is usually arranged in the form of a
series of from four to nine transverse cords, the vasa efferentia,
and two longitudinal ones. The first of the longitudinal cords
forms the central canal extending through the length of the testis
and receiving spermatozoa either from the spermatic ampullae
or from branches extending to the same. The second longi-
tudinal duct is situated close to the median border of the meso-
nephros and crosses the vasa efferentia. In some plethodontids
this longitudinal duct is absent and the vasa efferentia run directly
to the renal corpuscles of their apparent origin. In Ascaphus
three or more branches of the vasa efferentia of one side are
connected with the longitudinal canal of the opposite kidney,
and India ink injected into the Wolffian duct of one kidney will
fill the vasa efferentia and kidney tubules of the opposite side.
The kidney shown in Fig. 99 has been injected in this way. It is
interesting that the only other amphibian known to show a fusion
of parts of the testicular nets of the two sides is the primitive
salamander, Hynobius lichenatus, as described by Yamagiva
(1924).

Primitively in both frogs and urodeles the spermatozoa were
passed by a series of vasa efferentia into renal corpuscles of the
mesonephros from which they made their way into the Wolffian
duct and cloaca. In some of the most primitive of living urodeles

274 THE BIOLOGY OF THE AMPHIBIA

the mesonephric tubules fail to reach the Wolffian duct but
extend posteriorly to empty independently into the cloaca.
Yamagiva (1924) has shown this to be the condition in both
sexes of Megalobatrachus and in the male Hynobius. In the

Fig. 99. — The vasa efferentia of Ascaphus. The Wolffian duct of the right
kidney has been injected with ink. Transverse ducts connect the vasa effer-
entia of the one side with a longitudinal canal of the opposite kidney. Hence
ink injected into the right Wolffian duct makes its way into the vasa efferentia
of the opposite kidney. W.D., Wolffian duct; M.D., Mullerian duct; V.E., vasa
efferentia; L.C., longitudinal canal; T, right testis; F.B., fat body.

female a few of the tubules empty into the Wolffian duct, while
others open into the cloaca. It is remarkable that in the closely
related Onychodactylus some of the tubules of the male fuse to
form a common duct opening into the cloaca, while others join
the Wolffian duct. Onychodactylus has been derived from Hyno-
bius and yet it shows a theoretically more primitive condition

THE UROGENITAL SYSTEM

275

of these ducts. Such facts when considered in their phylogenetic
perspective show that evolution has not always proceeded in a
progressive manner. Possibly the more primitive condition of
the mesonephric ducts of Onychodactylus may be explained as
the retention of a juvenile character which is passed over in the
ontogeny of Hynobius.

The testes of Amphibia are shorter than the kidneys and the
vasa efferentia empty into only a limited number of the glomeru-
lar capsules. Such capsules are usually reduced in size, and their
renal corpuscles as well as their nephrostomes are lost. The
cells in the proximal convoluted portion of the tubules leading
from these capsules become ciliated in some forms such as
Necturus (Chase, 1923), while the distal convoluted portion of
the same tubules becomes very wide. In some Salientia the vasa
efferentia appear to empty directly into the transverse collecting
tubules, apparently because the glomerular capsules have been
lost and the nephric tubules shortened. Radical differences in
the modification of these ducts may exist between closely related
species, as, for example, between the two European frogs Rana
esculenta and R. fusca. Radical changes in the mesonephric
tubules transversed by spermatozoa do not lead in some
Amphibia, such as Necturus, to any alteration in the form of the
kidney, but in most urodeles the anterior part of the mesonephros
is narrowed as if to facilitate a short passage across the kidney
for the male sex products.

Both frogs and urodeles show a tendency to reduce the posterior
part of the testicular net. In Necturus and Proteus, only the two
anterior vasa efferentia are functional, while Chase (1923) records
one specimen of the former in which only the most anterior
transverse duct of the testicular net was utilized. The disco-
glossid toads, although primitive, show an extreme stage in this
restriction of function to the anterior vasa efferentia. In the
adult male Discoglossus and Alytes the first and second vasa
efferentia, which alone are functional, reach the Wolffian duct
by crossing entirely anterior to the kidney. Probably a portion
of this duct includes one or more modified mesonephric tubules
which have completely freed themselves from the rest of the
kidney. The collecting tubules of the mesonephros of these
genera form a common duct which resembles a ureter of higher
vertebrates in serving as a duct for the kidney secretions alone,
but it differs from a true ureter in not having arisen from the

276

THE BIOLOGY OF THE AMPHIBIA

Wolffian duct. In the dipnoans it is the posterior part of the
testicular net which is modified to make a short circuit to
the Wolffian duct. Rudiments of the testicular net appear in the
females of some Amphibia, but like the Miillerian ducts in the
male they never attain a functional state. In some Salientia,
such as Rana sylvatica and Alytes, the caudal portion of the
Wolffian duct of the male is enlarged to form a saccular reservoir
for the spermatozoa, the vesicula seminalis. This would seem to
permit the use of a large amount of sperm in a short time by
these species.

Urinary Bladder. — The renal ducts of Amphibia are not
enlarged to form reservoirs for the urine as in some fish. On the
other hand, an evagination of the ventral wall of the cloaca
immediately adjacent to the openings of the Wolffian duct
extends forward into the abdominal cavity and functions as a
urinary bladder. This bladder may be cylindrical as in Proteus
or Amphiuma, bicornuate as in salamandrids and various frogs,
or nearly two-lobed as in certain discoglossids (Field, 1894).
It reaches its largest size in the aquatic Amphiuma and in some
terrestrial species such as Hydromantes and Bufo. In the latter
it would seem to function, as stated above, as a reserve supply
of water to delay desiccation. The bladder is held in place by
sheets of peritoneum. It is well provided with smooth muscle
and is closed by a sphincter which is frequently released by frogs
and toads when roughly handled. The release of the fluid from
the bladder lightens the animal and facilitates its escape.

Sex and Its Modification. — In the above description of the
urogenital organs various similarities between the two sexes were
noted at certain stages of development. The earlier the stage
selected the more difficult it becomes to distinguish between the
sexes. In fact, for a considerable period the gonads and associ-
ated structures of the two sexes are identical except for assumed
differences in the chromatin material which are often not demon-
strable cytologically. Sex is, nevertheless, determined very
early. During the maturation of the germ cells, sex differences
may be seen in the chromosomes of the developing sex products
(Fig. 8) . Two kinds of germ cells occur in the male of some species
of Rana, one male-determining, the other female-determining,
but in the toad only one kind has been demonstrated (Brambell,
1930). Iriki (1930) was unable to distinguish a heteromorphic
sex chromosome in Hyla arborea japonica and concluded that the

THE UROGENITAL SYSTEM

277

male tree frog was homozygous in respect to sex. Whether there
are two kinds of sperm cells in the male or two kinds of eggs in
the female, sex is, nevertheless, determined at the time of fer-
tilization by genetic factors carried by the chromosomes of the
uniting germ cells. Once the sex has been established, environ-
mental factors may intervene to reverse the result completely
and permit the opposite sex to come to full development.

The germ cells when first distinguishable are found in the
entoderm of Salientia and some urodeles (Bounoure, 1925) but
in the mesoderm of other urodeles (Humphrey, 1929). In Rana
sylvatica at the time of hatching they form a median ridge above
the mesentery. Witschi (1929) has traced the history of these
cells. At the time the external gills are being reduced the ridge
divides into two rows of germ cells, the future gonads. A series
of cells migrate from the blastema of the mesonephros and enter
the gonads. These are the rete cords which come to occupy a
central position in the undifferentiated gonad while the germ
cells form the cortex. Sex is first distinguishable when the germ
cells migrate from their more peripheral position and become
surrounded by rete cells which are to form the seminiferous
tubules of the male. In the female the germ cells transform
into ovocytes and eggs without losing their position in the cortex.
At about the time of metamorphosis some rete cells in the male
form the vasa efferentia connecting the seminiferous tubules
with the mesonephros, while in the female they are transformed
into the ovarian sacs without extending to the kidney. Witschi
concluded from this and earlier studies that the rete cords in
the center of the gonad contain the male differentiating system.
If it becomes active it causes the germ cells to migrate from the
cortex into the medulla of the gonad and to transform into
spermatogonia. If it is not active, other substances in the cortex
and presumably in the follicle cells transform the germ cells
into ovogonia. Witschi (1929) subjected Wood Frog tadpoles
to high temperatures and produced either males or females trans-
forming into males, but he obtained no typical females. In
this case heat had apparently destroyed or inhibited the female
determining substance in the cortex, releasing a compensatory
growth of the medulla and its subsequent differentiation into
rete and seminiferous tubules. Piquet (1930) has confirmed
Witschi and has shown that high temperatures would tend to
change genetic females into males. In both Rana temporaria

278

THE BIOLOGY OF THE AMPHIBIA

and Bufo vulgaris & temperature of 25° produces a very high
excess of males. A temperature of 20° is neutral in the toad but
has a slight masculinizing effect in the frog.

In the toad the reversal of sex has apparently been accom-
plished but under different conditions. In the tadpole of Bufo,
the anterior portion of each gonad becomes enlarged and in the
adult, forms the Bidder's organ, a structure which has been
frequently compared to a rudimentary ovary. Harms (1926)
and Ponse (1926) found that removing the testes caused the

Fig. 100. — Sex reversal in a toad. Three and a half months after removing
the testes of the adult toad, part of the Bidder's organ has developed into an
ovary. B., urinary bladder; F.B., fat body; Liv., liver; Ov., rudimentary ovary.
{After Harms.)

Bidder's organ to develop into a functional ovary (Fig. 100)
If Bufo is assumed to be hermaphroditic, this would not be a
case of sex reversal but merely a growth of the ovary after the
inhibitory effect of the testes was removed (Ponse, 1927). The
cells of Bidder's organ, however, have the appearance of indiffer-
ent germ cells which, although potential sperm, are transformed
into ova by the conditions of the experiment.

Sex reversal has also been accomplished in salamanders in a
more decisive manner. Burns (1925) joined pairs of Ambystoma
together at an early stage before sex differences in the gonads were
visible. When the salamanders developed, the sex of the mem-

THE UROGENITAL SYSTEM

279

bers of each pair was always the same. As it was very unlikely
this could have come about through the chance selection of
individuals of the same sex, a sex reversal would seem to have
occurred in some instances. Humphrey (1929a) implanted the
preprimordium of the gonad of one sex into the embryo of
another after removing the corresponding gonad preprimordium
from the latter and found that it usually differentiated according
to the sex determination of the donor. Later a modification or
sex reversal of the graft or host gonad may be effected. When an
ovary or testis of similar size and species developed together in
an animal it was always the ovary which suffered modification.
A hormone from the testis apparently exerted an inhibitory
influence on the growth of the ovarian cortex very similar to the

Fig. 101. — The urogenital systems of four adult frogs, Rana temporaria,
representing stages in the transformation of females into males. K., kidney;
M.D., Mullerian duct; Ov., ovary; S.V., seminal vesicle; T., testis; W.D„, Wolf-
fian duct. {After Witschi.)

action of heat in the case of the Wood Frog, and further changes
in the male direction were a result of the cessation of cortical
activity. If the gonad developed from a male donor was small
in size or retarded in development, it was not able to dominate
the ovary, but on the other hand, it underwent a partial sex rever-
sal. It would thus seem that there are both male and female
determining substances in the developing gonads. Amphibia
pass through an indifferent and apparently later a bisexual state
before genetic factors give the ascendency to the tissues which
shape the germ cells into either ova or sperm. Up to a certain
stage various environmental factors can reverse this dominance,
and gonads of the opposite sex will develop. This shift of
balance is not, however, transmitted to the next generation.
Female frogs which have changed into males (Fig. 101), when
mated with normal females produce only female offspring (Crew,

280

THE BIOLOGY OF THE AMPHIBIA

1921). The genetic constitution of the germinal material is not
changed, although its expression in any one generation may be
modified.

Segmentation of the Gonads. — The gonads of frogs shortly
after the penetration of the rete cords exhibit a certain lobulation
which has been considered evidence of a primitive metamerism
perhaps harking back to the first vertebrates which presumably
had metamerically divided body - cavity and gonads. The
suggestion is rendered the more probable in that the testes of
caecilians are divided into a series of segments connected by the
central longitudinal canal. Other elongate-bodied Amphibia,
such as Siren and Amphiuma, have the testis undivided and hence
the segmentation is not merely a consequence of body form.
Many plethodontids and salamandrids have the testis divided
into several well marked lobes which have been described as
multiple testes. Humphrey (1922) has shown that each lobe
represents a center of active spermatogenesis, the region between
lobes merely an area which has produced spermatozoa and has
delayed in the formation of a new spermatogenetic cycle. The
lobes thus represent waves of spermatogenesis which move
forward from year to year. There may be considerable irregu-
larity in the formation of the lobes. The testes of frogs some-
times exhibit a certain gonomery during their ontogeny. This
has no relation to the lobulation of the urodele testis but may be
reminiscent of the caecilian condition. The lobulation in uro-
deles apparently has no phylogenetic significance, but it is inter-
esting that only two closely related families of salamanders
should have developed this type of testicular modification.

Fat Bodies. — The gonads of Amphibia have certain nutriment
requirements which are often violated under laboratory con-
ditions. Inanition prevents sexual differentiation in immature
animals and causes degeneration of the mature germ cells in the
adult. Amphibia are provided with conspicuous paired fat
bodies as a reserve supply of nutriment for the gonads. The
fat bodies in urodeles are usually in the form of a pair of bands
enveloped in folds of peritoneum and lying parallel to the kid-
neys between them and the gonad. In the Salientia the fat
bodies are fingerlike structures situated at the anterior end of
the gonad. In the caecilians they are more extensive than in
other Amphibia and form a series of lobes parallel to the genital
organs. In both frogs and toads the fat bodies are known to

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281

arise from the anterior part of the developing gonad, although
this has been denied by some investigators (Kennel, 1913).
They reach their maximum size in the fall before hibernation
and their minimum size after egg laying. Partial castration
causes the fat bodies to hypertrophy (Dubois, 1927). Removal
of the fat bodies causes a degeneration of the sexual products,
the most advanced stages degenerating first (Adams and Rae,
1929). The fat bodies are therefore necessary for maintaining
the health and normal development of the gonads.

Ovulation. — The eggs lie in the cortex of the ovary and each
egg during the growth period is surrounded by a layer of follicle
cells which is enclosed by a vascular network. A thin vitelline
membrane covers the surface
of the mature egg. This
membrane is duplex, an outer
portion, the zona pellucida,
having been produced by the
follicle cells (Fig. 102) and an
inner portion, the zona radi-
ata, by the egg itself. The
eggs project into the lumen
of the ovary, and the outer
surface of the latter is covered
with peritoneum.

During the breeding season
each egg breaks through the
wall of the ovary at the point
where its stalk joins the ovarian epithelium. A small hole ap-
pears in the peritoneum and the egg in squeezing through this
aperture may be forced into an hourglass shape (Smith, 1916).
The egg when free in the peritoneal cavity is said to be carried
to the open mouths of the Miillerian ducts by ciliary action.
Smith (1916) finds few cilia present in either Rana pipiens or
Cryptobranchus, however, and it seems possible that eggs are
forced into the oviducts partly by suction; the mouths of the
oviducts being attached to the pericardium would gape open at
each heart beat. The movements of the female would also tend
to squeeze the eggs through the outlet. Fertilization in some
salamanders takes place near the mouth of the oviduct, the egg
having thrown off the polar bodies while within the ovary or
peritoneal cavity. Weber (1922) suggests that the fertilization

Fig. 102. — A developing ovocyte of
Cryptobranchus. A section through the
ovarian wall of a 26 cm. specimen. C.W.,
cyst wall; E.P., inner epithelial membrane
of the ovarian wall; Fol., follicle cell; N.,
nucleolus; V., vitelline body. (After Smith.)

282

THE BIOLOGY OF THE AMPHIBIA

of the eggs of Salamandra atra may occur in the peritoneal cavity
and that the death of the eggs which reach the oviduct last may
be due to excessive polyspermy, for as many as 200 spermatozoa
may be found in a single egg destined to degenerate.

The eggs are propelled through the oviducts by the action of
cilia. The oviducts are lined with either mucus-producing cells
as in the newt or with tube-shaped glands as in Rana. The
cilia usually lie on the summits of ridges which run more or less
the length of the oviduct. As the eggs progress they become
covered with mucus or similar gelatinous material. In most
Amphibia the distribution of the glands or mucous cells is not
uniform throughout the oviduct, and, as shown by Lebrun (1891),
the anterior, middle, and posterior regions of the oviduct may
differ considerably in muscular, glandular, and ciliary equipment.
Further, the glandular tubules in the anterior part of the oviduct
may differ in length or character from those in the posterior part.
This structural differentiation of the oviduct is reflected in the
egg capsules which may be as many as three well-defined ones,
aside from the vitelline membrane. Where the eggs pass
continuously through the oviduct as in Bufo, the outer capsule
may be a string of uniform width; if the eggs are held in the
posterior part of the oviduct and finally ejected rapidly, the spawn
may form a clump surrounded by a single saclike capsule. It is
remarkable that such apparently trivial differences are frequently
uniform throughout natural groups of species and may be used
as a ready means of identification. The egg sacs of the Hyno-
biidae, for example, cannot be confused with those of other
salamanders.

There is some evidence that mucus may be secreted without the
direct contact of the egg (Wetzel, 1908). Frogs have been found
with egg capsules but no eggs in one of the oviducts (Voss, 1927).
Further, some species, such as the tree frog, Phyllomedusa,
normally lay empty egg capsules which may be used in the
construction of its "nest." Frogs that build "foam nests"
may produce gelatinous nest material before the eggs are laid,
and Limnodynastes tasmaniensis has been described as building
one foam nest entirely without eggs (Klingelhoffer 1930).

The gelatinous capsules of the eggs swell enormously when
brought in contact with water, and frogs which have been
prevented from laying have been described as bursting from the
rapid imbibition of water by the uterine eggs (Nussbaum, 1908).

THE UROGENITAL SYSTEM

283

Fertilization. — Fertilization is external in most frogs; only
two genera are known to impregnate the eggs within the oviducts.
On the other hand, all salamanders except the primitive Hyno-
biidae and Cryptobranchidae (apparently the Sirenidae as well)
produce spermatophores, which are usually picked up by the
female, although they may be transmitted directly into her
cloaca. It is interesting to trace the evolution of the sperm-
receiving mechanisms of the female, for it follows closely the
phylogenetic order. In Ascaphus, one of the most primitive
frogs, the cloaca is extended into a highly vascular tube which
may be bent forward by the contraction of the rectus abdominis.
The tip of this copulatory organ is inserted into the cloaca of
the female during amplexus, and the oviducts become well
provided with spermatozoa which make their way between the
mucous folds, there being no special organ for receiving them.
The Gymnophiona also practice internal fertilization and for
this purpose are provided with a muscular extension of the
cloaca which, as in the case of the "tail" of Ascaphus, may
bear horny spines, these being visible only when the organ is fully
everted. (Fig. 154C). Unlike Ascaphus, the male caecilians
withdraw their cloacal extensions entirely within the vent when
not in use, a special retractor muscle making this possible.
Caecilians agree with Ascaphus and differ from urodeles in lack-
ing a spermatheca or sac in the female cloaca for reception of the
sperm.

Structure of the Cloaca. — The spermatophore of the sala-
manders is produced by the combined action of two sets of glands :
the pelvic gland lying in the roof and sometimes in the upper
portion of the cloaca of the male, and the cloacal glands which
cover the walls of the cloaca and are most conspicuous on the sides
where they form rows of papillae or in some species villosities.
In the posterior corner of the cloaca there empties a third set of
glands, the abdominal, which receive their name from the fact
that in some species of salamandrids they extend forward over
the roof of the cloaca into the abdominal cavity. The abdominal
glands may empty outside of the cloaca on small papillae as in
some newts (Heidenhain, 1892), or on a low papilla on either
side of the posterior corner of the cloaca as in Plethodon cinereus.
Since these glands may or may not empty within the cloacal
lips they seem to play no part in spermatophore formation but
apparently serve to stimulate the female during courtship.

284

THE BIOLOGY OF THE AMPHIBIA

D.GI.

In the cloaca of the female salamander all three sets of glands
may appear, although here they have different functions. The

pelvic gland serves as a res-
ervoir for the spermatozoa
which migrate from the dis-
integrating spermatophore
held between the lips of the
cloaca to these tubules in the
roof of the cloaca (Noble and
Weber, 1929). The cloacal
glands which are present in all
ambystomids, salamandrids,
and primitive plethodontids,
may play some part in egg-
capsule formation. The ab-
dominal glands are also de-
veloped in female newts.
They are present in Amby-
stoma,Necturus,and Eurycea,
although apparently rudimen-
tary and non-functional.
Their homologies with the
male glands have been estab-
lished by transplanting a testis
into the body of the female.
The spermatheca in the newt
then changes into the pelvic
gland, the rudimentary ab-
dominal glands into a func-
tional organ (Beaumont,
1928). It is interesting that
in Desmognathus, where
neither abdominal nor cloacal
glands are present even as
rudiments in the female, the
same operation causes these
two glands to sprout de novo
from the undifferentiated epi-
thelium of the cloaca of the adult female (Noble and Pope, 1929).
Thus, even in the higher plethodontids the abdominal and cloacal

Fig. 103. — Diagrammatic sagittal sec-
tion of the cloacas of three salamanders
to show the evolution of the spermatheca.
Anterior end on the left. (Based on data
from Kingsbury and from Dieckmann.)
A. Necturus. Spermatheca tubules nu-
merous and opening on the roof of the
cloaca. B. Ambystoma. Tubules less
numerous and opening into a common
duct. C. Desmognathus. Showing fur-
ther reduction and modification of the
tubules, also loss of dorsal and ventral
glands. C.T., common tube of spermathe-
ca; D.GI., dorsal gland; Sp., spermatheca;
V.GL, ventral gland.

THE UROGENITAL SYSTEM

285

glands are potentially present although unrepresented by visible
rudiments.

Evolution of the Spermatheca. — The spermatheca, or modified
pelvic gland of the female, undergoes a progressive change during
phylogeny. In the salamandrids and Necturus, it is represented
by numerous tubules which empty like the pelvic gland of the
male on the roof of the cloaca. In the ambystomid Rhyacotriton,
the area on which some of these tubules empty is evaginated from
the roof of the cloaca as a shallow pocket. In the Plethodontidae
this pocket has become a duct into which a number of tubules
empty. Each of the latter ends blindly in a saccular enlarge-
ment, in which the spermatozoa come to rest. The more
specialized and terrestrial plethodontids exhibit a reduction in
number of the spermathecal tubules emptying into the common
duct (Fig. 103). The only exception to this progressive change
in cloacal apparatus within the Plethodontidae is found in the
Four-toed Salamander, Hemidactylium. This species fails to
develop a central tube and moreover retains a rudiment of the
abdominal gland of the female. Nevertheless, its tubules are
only 3 or 4 (Dieckmann, 1927) instead of 15 to 25 as in primitive
plethodontids, and it lacks the cloacal gland rudiment which is
present in the female of Gyrinophilus and Eurycea. Hence the
cloaca of Hemidactylium may be considered a further specializa-
tion rather than a retention of a primitive type.

In the evolution of the common tube out of a diverticulum of
the roof of the cloaca, not all of the pelvic gland tubules were
involved. Transplanting a testis into the adult female Des-
mognathus causes some pelvic gland tubules to sprout de novo
from the epithelium of the roof of the cloaca. It is interesting
that the abdominal and cloacal glands which are closely con-
trolled by the testicular hormones in Desmognathus should appear
in both sexes in more primitive salamanders. This subject will
be considered further in the discussion of the endocrine organs.

Identification of Sex. — The different glandular equipment of
the cloacas of the two sexes of most salamanders permits their
ready identification without dissection. The papillae within the
cloacal lips of the male are replaced by smooth folds in the female
(Fig. 104). The abdominal gland or its papillae are often visible
in the male. The spermatheca is usually heavily pigmented
even in the cave salamander, Typhlomolge. Hence a salamander
with smooth or folded cloacal walls without papillae but with a

286

THE BIOLOGY OF THE AMPHIBIA

dark pigment spot in the roof of the cloaca is a female. Some
female plethodontids, especially Plethodon, have a small papilla

Fig. 104. — The cloacal orifice of a male (A) and a female (B) salamander,
Desmognathus fuscus, showing the villosities which serve to distinguish the males
of most species of salamanders from the opposite sex. A.G., abdominal gland;
C.R., cloacal roof, region of pelvic gland; V., villosities of the cloacal glands.

which projects from the roof of the cloaca, obscuring the view of
the spermatheca. Males are identifiable not only by their papil-
lose cloacas but by their secondary sexual characters. There

THE UROGENITAL SYSTEM

287

are sexual differences also in the cloacas of the hynobiids and
cryptobranchids which have a simpler glandular equipment
than the salamanders producing spermatophores. The pelvic
gland has been compared with the prostate of mammals. Its
secretion, which may be readily observed in the living animal, is
white, and serves to hold the spermatozoa together in a clump
on the top of a gelatinous base produced by the cloacal glands.
From its position the pelvic gland may be homologous to the
prostate, although it has different functions. The enlarged
glands within the cloacas of Salientia may possibly be homologized
with the pelvic glands, although their function is not definitely
known. In the Salientia sex may be identified by the presence
of the secondary sexual characters discussed in Chap. V.

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Adolph, E. F., 1927: The excretion of water by the kidneys of frogs, Amer.

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Beaumont, J. de, 1928: Modifications de l'appareil uro-genital du Triton

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XCVIII, 563-564.

Bensley, R. R., and W. Brooks Steen, 1928: The functions of the differ-
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Bieter, R. N., and A. D. Hirschfelder, 1929: The role of the glomeruli as

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Bounoure, L., 1925: L'origine des gonocytes et revolution de la premiere

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Burns, Robert K., 1925: The sex of parobiotic twins in Amphibia, Jour.

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Dieckmann, J. M., 1927: The cloaca and spermatheca of Hemidactylium

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Field, H. H., 1894: Morphologie de la vessie chez les batraciens, Bull.

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Gottschalk A., and W. Nonnenbruch, 1923: Die Bedeutung der Leber

fur die Harnstoffbildung, Arch. exp. Path., XCIX, 261.
Gray, P., 1930: The development of the amphibian kidney. Part I. The

development of the mesonephros of Rana temporaria, Quart. Jour.

Micr. Sci., LXXIII, 507-546, pis. 27-31.
Haan, I., and A. Barker, 1924: Renal function in summer frogs and winter

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Hall, R. W., 1904: The development of the mesonephros and the Mullerian

ducts in Amphibia, Bull. Mus. Corny. Zool. Harvard, XLV, 31-125, 8 pis.
Harms, Jurgen W., 1926: "Korper und Keimzellen," Berlin.
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in the renal portal and renal veins, Amer. Jour. Physiol., LXXXVI,

331-339.

Heidenhain, M., 1892: Notiz betreffend eine rudimentare Druse bei den
Weibchen der einheimischen Tritonen, Anat. Anz., VII, 432-435.

Howland, R. B., 1920: Experiments on the effect of removal of the prone-
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Humphrey, R. R., 1922: The multiple testis in urodeles, Biol. Bull., XLIII,
45-67.

— , 1929: The early position of the primordial germ cells in urodeles:

evidence from experimental studies, Anat. Rec, XLII, 301-314.

, 1929a: Studies on sex reversal in Amblystoma; II. Sex differentia-
tion and modification following orthotopic implantation of a gonadic
pre-primordium, Jour. Exp. Zool., LIII, 171-221, 4 pis.

Iriki, S., 1930: Studies on amphibian chromosomes; 1. On the chromosomes
of Hyla arborea japonica Guenther, Mem. Coll. Sci. Kyoto Imp. Univ.,
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Kennel, Pierre von, 1913: Les corps adipolymphoides des batraciens,

Ann. Sci. Nat. Zool, 9th Ser., XVII, 219-254.
Klingelhopfer, W., 1930: Terrarienkunde, Lief. 15-16. Stuttgart.
Kuki, S., 1929: The ratio of the elimination of the dyes from both the

glomeruli and tubules, Proc. Imp. Acad. Tokyo, V, 393-395.
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batraciens indigenes, La Cellule, VII, 417-484, 6 pis.
Liang, T. J., 1929: tiber die Harnbildung in der Froschniere XVIII Mitt;

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Abschnitten, Pflugers Arch., CCXXII, 271-286.
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Riesensalamander, Zeitschr. Anat. Entw., LXXXVIII, 88-111.
Noble, G. K., and S. H. Pope, 1929: The modification of the cloaca and

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Noble, G. K., and J. A. Weber, 1929: The spermatophores of Desmognathus
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Rana esculenta, Arch. ges. Physiol., CXXIV, 100-111.

Oliver, J., and S. Eshref, 1929: A mechanism of conservation in the kid-
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Piquet, J., 1930: Determination du sexe chez les batraciens en fonction de
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Ponse, K., 1926: Changement experimental du sexe et intersexualite chez
le crapaud (nouveaux resultats), Compt. rend. Soc. Physiol. Hist. Nat.
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, 1927: L'evolution de l'organe de Bidder et la sexualite chez le crap-
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Przylecki, J., 1922: L'echange de l'eau et des sels chez les amphibiens,
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Richards, A. N., and Carl F. Schmidt, 1924: A description of the glomeru-
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Voss, H., 1927: Wodurch wird die Bildung der Gallerthullen des Froscheies
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Hok. Imp. Univ., XV, 37-82.

CHAPTER XIII

THE ENDOCRINE GLANDS

The coordination of the activities of the various organs of the
body may be brought about either through nervous impulses
transmitted along nerve tissue or by chemical substances set free
in the circulation. The latter are the hormones, and the best
known are produced by the endocrine glands. These glands of
internal secretion are found in various parts of the body. They
have frequently changed their form and character during phy-
logeny, and in some instances their endocrine functions seem to
have been secondarily acquired. The effects of their products
control many types of form and function and range from influ-
encing the rate of development, the coloration of the skin and the
growth of the secondary sexual characters to the appearance of
various types of behavior. Several of the endocrine organs are
duplex, having arisen from tissue of totally different origin.
They are functionally closely correlated among themselves, the
stimulation of one organ leading to a change in the activity of
another. This phenomenon makes it especially difficult to
analyze the specific functions of any one organ, for its extirpation
or transplantation leads to changes in the others. The study
of the internal secretions has attracted many investigators in
recent years, but the functions of several of the organs are still
incompletely known. Probably some tissues not united into
discrete endocrine organs discharge hormones into the blood
stream, there to regulate the activities of other parts of the body.
A good example is the small intestine with its hormone secretin,
discussed in another chapter. Again, waste products of metabo-
lism, such as carbon dioxide, may affect the respiratory centers
in the brain. As discussed in the chapter on respiration, these
centers control the breathing movements of Amphibia, increasing
the rate according to the need. Hormonal or parahormonal
substances which are not produced by definite endocrine organs,
however, are considered in other chapters.

290

THE ENDOCRINE GLANDS

291

The secretions of the endocrine organs often produce reactions
similar to those accomplished by the nervous system alone. The
nervous system is a more rapid and precise means of coordination,
and hence where speed of response is needed, as, for example, in
the color changes of certain tree frogs, the nervous component
plays the more important role in coordination. Where con-
tinuous activity is required, however, as in digestion, circulation,
or metabolism, a chemical control has decided advantages
over a nervous regulation. The two systems are often closely
interrelated, both stimulating the same effectors. In general,
endocrine control is slow and diffused; nervous control, swift and
precise. Nevertheless, the nervous system became well differ-
entiated as a discrete system in phylogeny before the endocrine
organs had evolved as definite structures.

Thyroid Gland. — The thyroid gland arises as a median out-
growth from the ventral wall of the pharynx although in the frog
its tissue appears to be derived from an ingrowth of ectoderm.
In Amphioxus and the Ascidians, this region is occupied by an
open groove of ciliated and mucus-producing cells which serve
to entrap food particles and drive them along to the intestine.
In the larva of Petromyzon this structure, the endostyle, is
present in a modified form, while in all higher vertebrates a
homologous growth, the thyroid, early separates from the phar-
ynx wall and develops a series of closed follicles which produce
a secretion of considerable importance in controlling the metabolic
level of the animal.

The thyroid was originally an unpaired structure, and this
condition is still maintained in the reptiles. During ontogeny
the thyroid of Amphibia becomes bilobed and the two halves
usually separate to move posteriorly and laterally to their final
position. In the adult frog the paired thyroids lie one on either
side of the hyoid apparatus just posterior to the postero-lateral
processes; in salamanders they have a more lateral position,
usually being found near the external jugular veins (Fig. 105).
There is, however, considerable variation in urodeles (Uhlenhuth,
1927), and accessory follicles appear in both frogs and salaman-
ders, a median group being the most frequent. The follicles
increase in size but not in number during larval life (Uhlenhuth
and Karns, 1928). At the time of metamorphosis there is a
marked increase in the secretory activity of the follicular cells,
and this is followed by a release into the blood stream of the

292

THE BIOLOGY OF THE AMPHIBIA

colloid contained in the follicles. During adult life the thyroid
undergoes certain cyclic changes, storing colloid in winter and
releasing it in summer (Sklower, 1925).

Thyroid and Metamorphosis. — The administration of thyroid
substance to man leads to an increased rate of metabolism, as
measured by oxygen consumption, also increased body tempera-
ture and pulse rate, emaciation, and nervousness. The first
result is obtained with amphibian larvae on treating them with
thyroid extracts (Helff, 1926; Belehradek and Huxley, 1927).
The treated larvae undergo a rapid transformation into the adult
form. The result is particularly striking in the case of such
species as Rana catesbeiana and Eurycea bislineata which normally

Fig. 105. — Diagram of the head of an adult Ambystoma showing position of
the thymus. E.B., epithelial bodies; T., thymus; Th., thyroid glands and asso-
ciated blood vessels. (After Baldwin.)

have a larval period extending over more than a year, since
changes begin from approximately a week to three weeks after
the treatment and are complete within the month. A single
feeding of thyroid gland is sufficient to bring forth all the changes
of metamorphosis in the case of some species.

Metamorphosis consists of many external and internal changes
in the organization of an amphibian. The more conspicuous
changes in salamanders include a loss of the gills and tail fin, a
shedding of the larval skin in one piece and its replacement by
the adult skin of different structure and usually color, a protrusion
of the eyeballs with the formation of lids, and finally a fusion of
the margin of the operculum to the underlying integument.
Wilder (1925) has described the many external and internal
changes of Eurycea bislineata at transformation, but not all of
these occur in other species of Amphibia. The larvae of frogs

THE ENDOCRINE GLANDS

293

lose their tail and larval mouth parts ; they also radically change
the shape of their head and body. Most tadpoles develop eyelids
on metamorphosing, but various pipids fail to do so. The com-
plete reduction of the gills is evidence of metamorphosis in most
salamanders but not in Siren (Noble, 1924). The limbs of
urodeles appear early in development and rarely show a structural
change during metamorphosis, but the rapid limb growth in
the tadpoles of some Salientia may be considered a metamorphic
change. Allen (1929) considers the degree of limb development
in tadpoles of Rana pipiens an accurate criterion of the extent
to which metamorphosis has advanced. Metamorphosis is a
combination of changes, most of which normally take place over
a short period, but in some species it may be extended over a
long period or may, in fact, not occur at all. In other words,
metamorphosis involves different changes in different species.

In metamorphosis there are two factors to be considered:
first, the tissue undergoing the change and, second, the mechanism
producing the change. Eyes (Uhlenhuth, 1917) or intestine
(Sembrat, 1925) transplanted from one individual to another
metamorphose synchronously with the host, but where transplant
and host are of different species the transplanted tissue retains
its own specific characters, those determined by its heredity.
As Allen (1918) and E. R. and M. M. Hoskins (1919) first showed,
tadpoles deprived of their thyroids are unable to metamorphose.
Thyroid extracts have no effect upon the segmentation of the
egg (Deutsch, 1924) or upon the very early larva. A certain
amount of differentiation must have taken place before the
thyroid hormone is able to act in the dramatic manner first
described by Babak (1913) and Gudernatsch (1913). In Rana
tadpoles the critical stage occurs shortly after the operculum
has grown back (Romeis, 1924). In the case of some perenni-
branch urodeles, such as Necturus and Proteus, this critical stage
never occurs; in others, notably Cryptobranchus and Siren, which
metamorphose only their skin, it occurs soon after hatching.
Still, in neither perennibranch nor frog tadpole is the ani-
mal's own thyroid sufficiently developed at this time to produce
metamorphic changes. Cryptobranchus and Siren have large
thyroids capable of inducing metamorphosis when fed to thyroid-
ectomized axolotls (Noble, 1924), but they fail to induce a com-
plete metamorphosis in their own bodies because most of the
tissues which in other salamanders usually undergo metamorpho-

294

THE BIOLOGY OF THE AMPHIBIA

sis here are not sensitive to the thyroid hormone. Jensen, Swin-
gle, and others found that thyroid substances induced no change
in Proteus or Necturus, although the thyroid of the latter is
capable of hastening metamorphosis when transplanted to Rana
tadpoles (Swingle, 1922). When Cryptobranchus and Siren are
subjected soon after hatching to thyroid extracts or thyroxin,
they shed their larval skin and assume the characteristic integu-
ment of metamorphosed salamanders. This change normally
occurs much later in the life of Cryptobranchus and Siren, and
presumably takes place under the influence of the salamanders'
own thyroids. It is evidence for the fact that the skin, alone of

all the tissues, which normally
metamorphose in related sal-
amanders, is in these forms sen-
sitive to the thyroid hormone.

Neoteny. — Urodele larvae are
frequently found sexually ma-
ture in nature, showing that the
development of the gonads is
f^not dependent on the thyroid
hormone. The removal of the
thyroid in mammals prevents
growth and leads to cretinism,
but the growth of the larvae of
both frogs and urodeles is un-
affected by this operation. In
the perennibranch Typhlomolge the thyroid may be absent,
but in view of the fact that none of the other perennibranchs
fully metamorphoses after thyroid treatment it appears
doubtful if neoteny in this genus can be attributed to the
loss or reduction of this organ. Blacher (1928) found that the
intestine of tadpoles was stimulated to metamorphic change
by weaker solutions of thyroid extracts than those necessary to
produce changes in the tail, while the latter responded to weaker
solutions than those required by jaws or trunk. Fontes and
Aron (1929) by using minimum doses of thyroxin showed that
the skin of tadpoles was more sensitive than the tail in the
species they were considering. The quantity of thyroid
hormone necessary to produce a metamorphic change varies
with the kind of tissue, the age of the animal, and the species
(see page 102).

A £

Fig. 106. — Sections of one of the
thyroid glands of a normal (A) and a
neotenic newt (B) , Triturus cristatus.
(After Kuhn.)

THE ENDOCRINE GLANDS

295

Neoteny in salamanders may be due not to a deficiency of the
tissues but to some factor which prevents the release of the thyroid
hormone into the circulation. As long ago as 1817 Spix suspected
that Proteus was the larval form of a terrestrial salamander.
On his memorable voyage to Brazil he carried a series of live
Proteus with him hoping that the warmer climate of the tropics
would induce Proteus to metamorphose. Cold apparently
inhibits the release of the hormone, for salamander larvae of
species which normally metamorphose frequently fail to do so
when they live at high altitudes. This is the case of the axolotl
of the Rocky Mountains, the neotenous larva of Amby stoma
tigrinum. There are other axolotls, larvae of the same or a
closely related species which live in warmer waters but due to
some inherited defect of the releasing mechanism remain larvae
for long periods. Such is the case of a Mexican axolotl and of
some tiger salamanders of New Mexico. Many newts (Fig. 106)
and other salamandrids have been found to develop neotenous
larvae at times. A large percentage of newts in the Woods Hole
region were found to be neotenous, but whether this was due to
an inherited defect of the releasing mechanism or to some environ-
mental factor is unknown (Noble, 1929). Zondeck and Reiter
(1923) found that calcium delayed the metamorphosis of tadpoles.
A lack of vitamines in the diet will prevent the metamorphosis
of Ambystoma larvae. Patch (1927) showed that larvae fed
only Enchytraei or beef muscle failed to metamorphose. The
addition of cod liver oil or yeast to the diet of the controls per-
mitted them to metamorphose successfully. There are, also,
various internal factors, such as the amount of insulin available,
which inhibit metamorphosis (Gessner, 1928). Hence, the
failure of a salamander to metamorphose may be due to any one
of several different causes.

Iodine and Metamorphosis. — It has long been known that the
thyroid gland is rich in iodine content. No other tissues of
craniates, in fact, contain so high a percentage. Swingle (1919)
found that iodine or its inorganic compounds administered to
toad and frog tadpoles induced a precocious metamorphosis
(Fig. 107), and Ingram (1929) has recently demonstrated that
the subcutaneous implantation of iodine crystals in the thyroid-
ectomized and hypophysectomized axolotl brought the same
result. In nature the iodine is received with the food or possibly
to a certain extent with the water, and the function of the thyroid

296

THE BIOLOGY OF THE AMPHIBIA

gland is to store it in the form of a colloid secreted by the follicle
cells of the gland. When the thyroid gland is removed and iodine
crystals are implanted, apparently other tissues are able to elabor-
ate an iodine compound effective in producing metamorphosis.

Kendall (1918) succeeded in isolating from the thyroid gland of
mammals a single crystalline substance containing iodine and

having the physiological properties of
thyroid extract. This, according to
Harington (1926), is an iodine derivative
of parahydroxyphenyl ether of tyrosine,
having the formula C15H11O4 N I4. The
iodine is apparently necessary for the
complete ossification of the skeleton,
since Terry (1918) found ossification de-
ficient in thyroidectomized tadpoles.
Once metamorphosis has taken place, the
tissues may still respond to the thyroid
hormone, since Belehradek and Huxley
(1927) found that oxygen consumption
was almost immediately increased by
injecting thyroid into the metamorphosed
Ambystoma. Gayda (1924), however,
3 was not able to find any effect of thyroid
feeding on adult frogs, but as Sembrat
(1925) found that larval intestines of
Pelobates transplanted into the metamor-
phosed frog underwent a transformation,
the thyroid hormone must have been cir-
culating in the tissues of this species.
Possibly Gayda's frogs were too old to
respond to treatment. The thyroid
hormone would seem to have an impor-
tant function throughout life, but in Amphibia it is especially
significant in its influence on metamorphosis.

Pituitary Gland. — The pituitary gland of Amphibia agrees with
that of teleosts in arising from a solid ingrowth of ectoderm
between forebrain and foregut (Fig. 108). It loses its connection
with the surface and becomes applied to the infundibulum, a
ventral diverticulum of the thalamus. The ingrowth does not
develop normally if the infundibulum is experimentally destroyed
(Smith, 1920), while the nervous diverticulum fails to differentiate

Fig. 107.— The effect of
iodine on metamorphosis.
The tadpole which was fed
iodotyrosine (A) had well
begun its metamorphosis in
fifteen days while the control
(B) fed tyrosine remained a
tadpole after forty-two days
oftreatment. (After
Swingle.)

PRIVATE LIBRARY OF
ALBERT G. SMITH
THE ENDOCRINE GLANDS 297

completely in the absence of the ingrowth. Hence, the two por-
tions of the gland, the hypophysial ingrowth and the infun-
dibulum, although of totally different origin, are mutually
dependent on one another for their differentiation.

Hyp.

Fig. 108. — Diagrammatic median sagittal section of a young frog larva showing
the hypophysial ingrowth. Hyp., hypophysis.

The hypophysial ingrowth of the pituitary differentiates into
three different parts: the pars anterior, pars intermedia, and pars
tuberalis (Fig. 109). The first is the largest and most conspicuous
portion. It lies not anterior but ventral and slightly posterior
to the others, but it receives its n^m,e frolh the homologous part
in mammals which has a more^anterior position. The pars inter-

bislineata. The nasal region is on the right. P. Ant., anterior lobe; P. Int.,
middle lobe; P. Post., posterior or neural lobe. (After Atwell.)

media is less vascular than the pars anterior and appears whitish
or opaque in the fresh animal. It lies chiefly dorsal to the pars
anterior in the adult. The pars tuberalis develops as a pair
of anteriorly directed processes on either side of the pars anterior
(Atwell, 1921). In the Salientia they become detached at the
time of metamorphosis to form separate plaques closely applied

298

THE BIOLOGY OF THE AMPHIBIA

to the base of the thalamus. In most urodeles they are retained
as processes, a separation having been reported only in one of the
newts (Sumi, 1926). The pars tuberalis reaches its maximum
size in the Plethodontidae, in a species of Plethodon, being five
times as large as the pars intermedia (At well and Wood worth,
1926). The infundibulum is sometimes described as the pars
posterior or pars nervosa of the pituitary. It is non-glandular
but frequently sacculated, as, for example, in Necturus.

Pars Anterior. — The pituitary produces a number of hormones.
The source of some of these has been traced by extirpation and
replacement methods to particular parts of the gland. From the
work on mammals the pars anterior is known to produce a sub-
stance which stimulates growth. When hypertrophy of this part
of the gland takes place in man it leads to gigantism before
puberty and to acromegaly after puberty. In tadpoles removal
of the pituitary results in a considerable retardation of their
growth (Smith, 1920). The restoration of the pars anterior alone
is sufficient to induce a return to the normal growth curve (Allen,
1928), while the implantation of the intermediate and posterior
lobes does not have this effect. Allen (1925) showed that the
extirpation of the pituitary stunted the growth of the limb bones
especially, and the effect was greater in frog than in toad tadpoles.
Frequent intraperitoneal injections of pars anterior extracts were
found by Smith and Smith (1923) to produce tadpoles twice the
volume of the controls. Gigantism has been produced in tiger
salamanders by feeding anterior lobe substance (Uhlenhuth,
1920). The giant larvae of frogs and urodeles sometimes found
in nature, however, are usually individuals which have failed to
metamorphose due to the non-functioning of their thyroid appara-
tus and hence are individuals which have prolonged the period
of larval growth.

The anterior lobe of the pituitary exerts an important control
over metamorphosis by influencing the growth and develop-
ment of the thyroid gland. This has been indicated in much
of the work on metamorphosis but was especially well shown
recently in the case of the tadpoles of Rana and Bufo by Allen
(1927). There is no accumulation of thyroid colloid in the
follicles if the anterior lobe of the pituitary is removed. Uhlen-
huth and Schwartzbach (1927) suggest that the hormone of the
anterior lobe may be also the factor which induces the release
of colloid from the thyroid follicles. Various investigations

THE ENDOCRINE GLANDS

299

have shown that the anterior lobe is unable to induce metamor-
phosis in larvae which have been deprived of their thyroids, but
the recent work of Spaul (1930) makes it appear probable that
during the later stages of larval life the anterior lobe may function
independently of the thyroid in inducing metamorphosis. The
extirpation of the thyroid causes an hypertrophy of both the
pars anterior and pars intermedia (Larson, 1927). The thyroid
would thus seem to exert normally a certain inhibitory effect
on the pituitary, while it in turn receives a growth-stimulating
hormone from the pars anterior of that organ. This stimulating
hormone is apparently produced by one type of cells in the
anterior pituitary, for cells of this type, the basophils, undergo a
rapid increase at the onset of metamorphosis (Allen, Torreblanca,
and Benjamin, 1929). Spaul and Howes (1930), however, con-
sider the oxyphils to be more concerned in metamorphosis
because the oxyphil region of the cattle pituitary is especially
iactive in inducing metamorphosis.

The pars anterior of the pituitary not only influences the body
growth and metamorphosis of amphibian larvae, but it also has a
specific effect on the growth and liberation of the sex products
of the adults. Daily transplants of fresh anterior pituitary
hasten sexual maturity in rats (Smith 1926), and similar treat-
ment causes Rana pipiens, el spring breeder, to lay its eggs in
October or November (Wolf, 1929). The simple act of insert-
ing fresh anterior lobe substance of Eurycea bislineata at frequent
intervals, through small slits made in the chin skin of adult
females of the same species, caused the latter to lay their eggs in
December and January (Noble and Richards, 1930), several
months before the normal breeding season. The eggs were laid
in typical position attached to the under side of stones placed
for that purpose in laboratory dishes. Since the females carry
spermatozoa in their spermathecae at this season, the eggs develop
without further assistance from the males. Wolf (1929a) found
that male frogs are also stimulated to sexual activity by fresh
pituitary substances injected into their lymph sinuses. The
effect of the implants is greater in the female than in the male
Bufo, however; more implants being necessary in the latter sex
to induce sexual activity (Houssay, Giusti, and Gonzalez, 1929),
and the same sexual difference appears to be true of some uro-
deles. Ablation of the anterior pituitary in the toad leads to
testicular atrophy (Houssay and Giusti, 1929). From this work

300

THE BIOLOGY OF THE AMPHIBIA

it would follow that the breeding-season rhythm of Amphibia is
under the direct control of the hormone of the pars anterior of the
pituitary. The hormone, in turn, may be under nervous control.
It is obvious that the breeding season occurs at certain favorable
seasons.

The discovery of a gonad-stimulating hormone has apparently
considerable practical value to students of Amphibia, for it
provides a ready means of obtaining embryological material
at any time of the year.

Pars Intermedia. — The pars intermedia of the amphibian
pituitary exerts an important control over the pigmentation. It
produces a hormone which induces both an expansion of the
melanophores and a contraction of the lipophores and possibly
also of the guanophores. As discussed in the chapter on the
integument, the pigment cells are also under nervous control
and further may respond directly to light. Nevertheless, the
pituitary hormone plays the chief role of color-tone regulator in
some species of Salientia. It was known from the early work of
Smith (1916) and Allen (1917) that ablation of the pituitary
induced a marked bleaching of the color in tadpoles. The
removal of the pituitary through the roof of the mouth is a simple
operation in the large-mouthed salamanders and it leads in a few
hours to the same lightening of color. Swingle (1921) showed
that intraperitoneal grafts of pars intermedia in hypophysec-
tomized Rana tadpoles brought a return of the original color or
even a more pronounced darkening. The pars intermedia and
posterior of the pituitary of cattle can also induce an expansion
of the melanophores of Amphibia (Atwell, 1919; Hogben and
Winton, 1922). The melanophore-expanding hormone, although
apparently produced by the pars intermedia, is able to make its
way into the pars anterior as well as into the pars posterior, for
Blacher (1927) and Smith (1925) have noted pigmentary changes
resulting from the injection of anterior lobe substance.

Pars Posterior. — The posterior lobe has certain specific effects
which would seem to be due to more than one hormone. It
has an important influence on the water equilibrium of both
larva and adult. Injection of posterior lobe extracts causes an
increased water intake, but repeated injections result in a loss
(Belehradek and Huxley, 1927a). Removal of the entire
pituitary in adult toads causes parts of the epidermis to form a
thickened horny layer (Puente, 1927). Marx (1929) found that

THE ENDOCRINE GLANDS

301

hypophysectomized Salamandra developed a similar pigmented
horny layer. In adult salamanders of several genera I have
found this development to occur chiefly on the under surface.
It would seem that this alteration of the skin was correlated with
a decreased water intake, for the entire integument of the
hypophysectomized salamanders appears drier than that of the
controls.

The removal of the whole pituitary results in a change in the
tonus of the cutaneous capillaries, which become strongly dilated.
Krogh (1926) suggests that the normal function of the pituitary
hormones is to maintain capillary tonus. Possibly the effect of
the postpituitary hormone on water regulation is produced
through its effect on the capillaries of the skin or kidney. Extracts
of the posterior lobe have a marked stimulating effect on the
smooth muscles of the mammalian uterus, but it is doubtful if
the effect is a general one on all smooth muscle (Hogben, 1927).
Allen (1929a) found that implantation of the posterior lobe in
adult frogs causes a contraction of the body walls lasting several
days. Spaul (1930) found that extracts of the posterior lobe
inhibit metamorphosis. In brief, all parts of the pituitary have
functions of great importance in the life of Amphibia. The
isolation of their specific autocoids, as has been accomplished in
the study of the thyroid, is still a matter for experimentation.

Pancreas. — The pancreas includes, besides the enzyme-
producing glands which pour their digesting fluids into the intes-
tine by way of the pancreatic ducts, a number of clusters of
epithelial cells which secrete a hormone directly into the blood
stream. These cell clusters, unlike the thyroid follicles, are
arranged in solid masses. They are called the " islets of Langer-
hans." Their hormone, insulin, regulates the amount of sugar
in the blood by facilitating the assimilation of sugar by the tissues.
If insulin is not present in the blood, glucose is neither oxidized
nor converted into glycogen but accumulates in the blood and
is excreted in the urine. Prevention of the normal functioning
of the islets of Langerhans leads to the disease diabetes which is
characterized by excessive amounts of sugar in the blood. Since
the discoveries by Banting and Best in 1922, the function of
insulin has been extensively investigated in mammals. Appar-
ently, injection of insulin in Amphibia has the same effect as in
mammals, if allowance is made for the lower body temperature
of these forms. Huxley and Fulton (1924) showed that the

THE BIOLOGY OF THE AMPHIBIA

effects were hastened in frogs by increasing the temperature up
to the normal maximum, and Olmsted (1926) has noted that
temperature increase speeded up the effect of insulin in the
toad. Aron (1928) finds that the internal secretion of the
pancreas is not manifest until the time of metamorphosis, but as
the glycogen of the liver does not vary greatly in relative amount

Fig. 110. — An adrenal organ of a frog. Left kidney of Rana catesbeiana
viewed ventrally showing the left adrenal organ, and associated structures.
Ad., adrenal organ; F.B., fat body; K,, kidney; T., testis; V., postcaval vein.

during ontogeny (Goldfederowa, 1926), other tissues may be
producing insulin. Recent investigations on mammals have
shown that insulin may be found in other tissues after the destruc-
tion of the pancreas. Hence, insulin is not a specific product of
the pancreas, although it would seem to be produced chiefly
by the islets of Langerhans.

Adrenal Organs. — The adrenal organs receive their name from
their proximityto the kidneys. In Salientia they form an irregu-

THE ENDOCRINE GLANDS

303

lar strip of yellow tissue adherent to the ventral surface of each
kidney, usually near the midline and closely associated with the
renal veins (Fig. 110). In Ascaphus they lie along the inner
edge of the kidneys, and this is the position of the bulk of the
organs in most urodeles. The adrenal organs resemble the
pituitary in being formed of two kinds of tissue of different origin
and function. The interrenal tissue, distinguished by the fatty
inclusions which give it the yellow color, develops from the
peritoneal epithelium either between the kidneys or anterior to
them near the midline. The chromaffin tissue, distinguished by
its intense staining in chromic salts and the granular inclusions

Fig. 111. — Development of the adrenal organ of Hypogeophis. Ao., aorta;
Jr., interrenal component of adrenal organ; N.T., nephric tubule; Pc.V., post-
caval vein; R.V., renal vein; Sy.C, sympathetic cells. (After Brauer.)

of its cells, arises from the neural tube at the time the sympathetic
ganglia are being formed (Fig. 111). In the mammals the
interrenal tissue forms the cortex, and the chromaffin the medulla
of their adrenal organs which are here, as in other amniotes,
isolated from the kidneys. In many urodeles adrenal tissue is
found anterior to the kidneys in small isolated masses frequently
associated with the sympathetic ganglia. In fact, chromaffin
cells have been considered merely modified sympathetic cells
and, like ganglia of the latter chain, they may receive sympathetic
fibers directly from the cord. Urodeles have a more diffuse
adrenal system than frogs or toads, but even in the latter the

304

THE BIOLOGY OF THE AMPHIBIA

adrenal tissue is usually broken up into a varying number of
segments (Vincent, 1898). There is more interrenal than
chromaffin tissue in Amphibia. Bonnamour and Policard (1903)
distinguish four kinds of cells in the adrenals of the frog. Pos-
sibly these represent different stages in the activity of the inter-
renal and chromaffin tissue.

The function of the interrenal tissue in Amphibia is unknown,
although there is evidence in mammals that its secretions influ-
ence the growth of the gonads. Precocious sexual maturity in
children has been attributed to a hypertrophy of this tissue in
certain cases. The interrenal tissue may also control the elimi-
nation of the acid end products of normal metabolism through
the kidneys (Swingle, 1927). The chromaffin tissue releases a
hormone, adrenalin, into the blood stream which apparently
has a non-specific effect of increasing the metabolism of the
tissues (Martin and Armistead, 1922). Feeding of adrenal tissue
to tadpoles increases their growth rate but has no effect on
metamorphosis (Herwerden, 1922). Destruction of the adrenal
organs in Salientia has been claimed not to have the fatal effects
well known in mammals (Giusti, 1921; Gley, 1927). The tissue,
however, is so widely distributed in the body cavity that its com-
plete removal presents great difficulty. In the toad Bufo marinus
Lascano Gonzalez (1929) has shown that some individuals which
survived the operation had some adrenal tissue present. Injec-
tion of adrenalin into frogs induces a contraction of the skin
melanophores and a rise in blood pressure due to the constriction
of the smooth muscle of the arterioles. Apparently in Amphibia,
as in mammals, adrenalin affects those organs innervated by the
sympathetic neurons and stimulates them in the same way.
It seems to act on the myoneural junctions rather than on the
sympathetic fibers, for the same results are obtained after the
fibers have been cut. The function of adrenalin in the behavior
of mammals is still a disputed matter (Hogben, 1927), although
there is evidence that it plays a part in some of the reflexes
associated with fright, where it is probably associated essentially
with the mobilization of bodily resources for the protective
reactions of the animal. In Amphibia, adrenalin may have an
influence on the normal metabolism by increasing the amount
of glucose in the blood through stimulating the liver to discharge.
Thus it increases the amount of sugar in the blood, while insulin
decreases it. The release of adrenalin in the blood would seem

THE ENDOCRINE GLANDS

305

to have some effect on pigmentation, for in some species injection
of adrenalin causes a contraction of the melanophores.

Adrenalin has been isolated chemically and found to be an
amine (organic base) closely related to the amino-acid, tyrosin.
Various substances closely allied to adrenalin and having similar
physiological effects have been synthetically produced.

Gonads. — The gonads, while primarily organs of reproduction,
release hormones into the blood stream which have an important
function in stimulating the growth and maintaining the develop-
ment of the secondary sexual characters. The latter include a
great variety of features in the Amphibia, ranging from the
familiar nuptial pads of male frogs and the broad tail crests of
male newts to obscure differences of teeth in salamanders and
tendon structure in frogs. The secondary sexual characters
include differences in red blood cell count, lung size, behavior
patterns, and many other structural and physiological differences
between the sexes. Some of these are discussed in a preceding
chapter. The utility of many secondary sex characters is not
always clear and their phylogeny presents a problem of special
interest.

Castration of sexually mature male newts results in a rapid loss
of the secondary sexual characters (Bresca, 1910). This change
is delayed by overfeeding (Champy, 1924) and by cold (Aron,
1923). Further, only a partial regeneration of testicular tissue
suffices to bring a return of the secondary sexual characters.
In frogs, because of these or other modifying influences, the
results of castration have not always been so marked. It seems
established, however, that the testis induces and maintains the
secondary sexual characters of the male. Welti (1925) and
Ponse (1923) induced the development of the nuptial pad in
female toads by testicular transplants, and Noble and Pope
(1929) have caused blunt bicuspid premaxillary teeth character-
izing the female Desmognathus fuscus to be replaced by elongate
monocuspid ones distinctive of the male by transplanting the
testes into the body of the adult female (Fig. 112). Testicular
transplants also induce the development of male behavior.
Brossard and Gley (1929) found that extracts- made from fresh
bull testes would induce the reappearance of the clasping reflex
when injected into frogs.

The testicular hormone of mammals is apparently produced
by the interstitial cells. In Amphibia these are stromal cells

306

THE BIOLOGY OF THE AMPHIBIA

Fig. 112. — Effect of testicular hormone on the teeth of a salamander. A.
The anterior teeth in the upper jaw of the female Desmognathus fuscus carolinen-
sis 220 days after spaying and transplanting a testis. The new premaxillary
teeth which have grown in, are elongate and directed forward in the form char-
acteristic of the male. The skull of the typical female (B) and a male (C), for
comparison. DENT, dentary teeth; MX, maxillary teeth; PAL., palatine teeth;
PMX, premaxillary teeth; VOM, vomerine teeth. {After Noble and Pope.)

THE ENDOCRINE GLANDS

307

surrounding the lobules of the testes. When the spermatozoa
are released from the lobule and the Sertoli cells undergo degener-
ation, the stromal cells increase by mitosis, change their form,
and exhibit lipoidal droplets and fuchsinophil granules in their
cytoplasm. Humphrey (1925) showed that all the secondary
sexual characters may be present in the male newt in which the
spermatozoa had not left the lobules and in which the interstitial
tissue had not yet made its appearance. It seems established
from the work of Champy (1924), Humphrey (1925), and Harms

(1926) that the source of the testicular hormone in Amphibia
is not to be found in the interstitial cells but rather in the sperm or
in the Sertoli cells.

Whether the testicular hormone be a by-product of spermato-
genesis or a substance released by the Sertoli cells, it can produce
its effect only on tissues which are sensitive to its action. Differ-
ences between two secondary sexual characters are due to
differences between the tissues and are not accountable to
the amount of hormone. Further, the development of some
secondary sexual characters may be due to other factors. Naka-
mura (1927) found that the cloacal papilla of certain European
newts could be made to develop in the female by treatment with
thyroid. The latter apparently affected adversely the growth
of the ovaries, and this, in turn, permitted the development of
the papilla which would appear to be a specific character normally
held in check by secretions of the ovary. In birds the function
of the ovary in supressing the male plumage is well known.
In frogs the ovary apparently controls growth of skin papillae and
influences the development of the oviducts. As stated above,
the growth and liberation of the sex products is under the control
of a hormone from the pars anterior of the pituitary. Aron

(1927) found that the spermatogenetic cycle of salamanders was
influenced by the elimination of spermatozoa. Further, the
grafting of immature testes into mature animals did not hasten
the cycle.

Parathyroids and Ultimobranchial Body. — The parathyroids
develop as epithelial growths from the ventral portion of the third
and fourth visceral slits. They appear late in larval life, in
Ambystoma apparently not until the time of metamorphosis
(Baldwin, 1918). Allen (1920) found that removing the thyroid
of toad tadpoles caused a marked hypertrophy of the para-
thyroids. There was no deposition of colloid or other histological

308

THE BIOLOGY OF THE AMPHIBIA

change suggesting that the parathyroids might assume the
functions of the thyroids. The parathyroids in mammals pro-
duce hormones which play an important role in calcium metabo-
lism, especially by controlling the concentration of calcium salts
in the blood. There is evidence that this may be true of Amphibia
as well (Waggener, 1929).

The ultimobranchial body arises as an epithelial growth from
the last gill pouch of each side. In urodeles that on the right side
is usually lacking, although it persists in Necturus and Amphi-
uma. The branchial origin of the structure suggests an endocrine
function but it rarely develops a colloid and shows no enlargement
during metamorphosis. In the adult it lies near the truncus or
larynx. Its function is unknown, although its widespread
occurrence throughout most vertebrates suggests that it must
have some functional significance. Wilder (1929) has described
the ultimobranchial body in a large series of urodeles and because
of its variability concluded that it probably had little or no
physiological significance.

Thymus. — The thymus gland arises from thickenings in the
dorsal portion of the visceral pouches. These thickenings become
epithelioid bodies which early lose their connection with the
pouches. In caecilians the first six visceral pouches of each side
produce thymus buds. In some salamanders, such as Ambys-
toma, the first five develop buds (Baldwin, 1918) but the first
two degenerate. The thymus of the adult accordingly is a
three-lobed structure, presumably formed by a fusion of the
three remaining buds of each side. In caecilians the first and
last pair of buds degenerate and the four remaining pairs fuse to
form a single element on each side. In some Salientia, according
to Maurer (1906), only the first two pairs of visceral pouches
take part in bud formation. The first pair degenerates and the
second pair develops into the definitive thymus which in the
adult lies under the skin caudal to the tympanic membrane and
is partly covered by muscle. In brief, while all except the most
posterior visceral pouches produce thymus tissue in the primitive
Amphibia, this power is greatly restricted in some salamanders
and in the Salientia.

The thymus glands, since they develop in much the same way
as the parathyroids, are assumed to have endocrine functions,
but these have not been clearly defined in either Amphibia or
mammals. Thymus feeding has had a variable effect both on

THE ENDOCRINE GLANDS

309

pigmentation and growth of tadpoles. The thymus is pro-
portionately larger during larval than adult life. In mammals
its persistence is associated with the retardation of sexual and
bodily development. In Amphibia the thymus functions in
producing lymphocytes, granulocytes, and also erythrocytes to a
certain extent. Speidel (1925) found that thyroid feeding
greatly stimulated the thymus of tadpoles and caused the growth
of lymphoid cells and their migration into the circulation.
Extirpation of the thymus in adult frogs apparently has little
effect on the animal's health (Agafonow, 1927), but it would be
interesting to perform the same operation during the breeding
season. Riddle has shown that the operation leads to serious
defects in the egg capsules of pigeons. The eggs of birds,
however, are much more advanced in structure than those of
frogs. The thymus may produce specific as well as general
effects in birds, but none of the specific effects has been estab-
lished in Amphibia.

Pineal Organ. — A well-marked pineal foramen is found in the
skulls of both branchiosaurs and lepospondyls, indicating that the
ancestors of modern Amphibia were equipped with a functional
median eye. In some tadpoles and even in a few adult frogs the
position of the pineal organ is indicated by a pigmentless, trans-
lucent spot on the forehead. The pineal arises in the embryos
of both frogs and salamanders as a diverticulum of the thalamus
which extends toward the integument of the forehead. The tip
enlarges to produce a vesicle which in Ambystoma may assume
the form of a rudimentary retina (Tilney and Warren, 1919),
having both pigment and an incipient differentiation of the cells.
Sense cells appear in the pineal organs of many Amphibia and
there are also ganglion and supporting cells (Vialli, 1929; Kleine,
1929). In the primitive Bombina, pigment is also formed, giving
further evidence of the original sensory nature of the pineal in
frogs. In many species, however, these differentiations fail to
appear, and the vesicle may fail to develop a well-defined lumen.

Nerve fibers usually appear in the stalk of the diverticulum
connecting the vesicle with the posterior commissure, but the
vesicle later becomes detached from the stalk and hence at this
stage can have no sensory function. In many aquatic Amphibia
(Triturus, Pipa, etc.), the vesicle is lacking. Most Amphibia
are nocturnal and hence might not be expected to have great
need of a median eye. It is interesting, therefore, to find that

310

THE BIOLOGY OF THE AMPHIBIA

the pineal has taken over other functions. In many species,
such as the cave salamander, Hydromantes italicus, the rudi-
mentary vesicle is primarily a secretory organ. In species where
the stalk persists, the latter also develops glandular functions.
The pineal organ of Amphibia has been reported to arise from a
paired diverticulum (Cameron, 1903; Riech, 1925). This is of
interest, for two diverticula, each with a terminal vesicle, develop
in Petromyzon. In the lizards it is the anterior one of these
which forms the parietal eye, which in some of these reptiles
apparently still functions as a light-receiving organ. Since the
two diverticula apparently fuse during the development of
Amphibia, it is not clear whether the pineal vesicle is homol-
ogous with the median eye of lizards or represents the posterior
of the two elements found in Petromyzon. Whether this vesicle
has any sensory functions in modern Amphibia is unknown.
The presence of sense cells in the structure may be taken as
evidence of some sensory function. The presence of lipoids,
however, and various other secretion products in the lumen and
in some of the cells (Vialli, 1929) shows that the organ has
secretory functions as well. The pineal is a rudimentary organ
which seems to have assumed endocrine functions.

The specific functions of the secretion of the pineal are not
clearly understood in Amphibia. McCord and Allen (1921)
found that feeding of pineal caused a temporary contraction
of the melanophores of Rana pipiens. Groebbels and Kuhn
(1923) confirmed the observation on another species of Rana.
But as McCord and Allen failed to observe definite changes in
toad tadpoles and as experiments with the pineal of urodeles
have been equally inconclusive, it would seem that the pineal
hormone was not an important regulator of pigmentary changes
in amphibian larvae. In mammals pineal extirpation induces a
precocious development of the gonads. Recently Schulze and
Holldobler (1926) have found that implantation of pieces of
beef pineal in tadpoles causes an acceleration of body growth;
and Addair and Chidester (1928) secured some evidence that
feeding desiccated pineal organ would hasten metamorphosis.
Further investigation is necessary before any specific function
can be assigned to the pineal gland of Amphibia.

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THE ENDOCRINE GLANDS

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THE BIOLOGY OF THE AMPHIBIA

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Gayda, T., 1924: Contribution a l'etude de la physiologie de la thyroide
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Gessner, O., 1928: Weitere Beitrage zur Frage der Beeinflussung der durch
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Giusti, L., 1921: Consequences de la destruction des surrenales chez le
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Groebbels, Franz, and E. Kuhn, 1923: Unzureichende Ernahrung und
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Gudernatsch, J. F., 1913: Feeding experiments on tadpoles; I, The influ-
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Harington, C. R., 1926: Chemistry of thyroxine, Biochem. Jour., XX,
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Harms, Jurgen W., 1926: "Korperund Keimzellen," Berlin.

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Helff, O. M., 1926: Studies on amphibian metamorphosis; II, The oxygen
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Herwerden, M. A. von, 1922: Der Einfluss der Nebennierenrinde des

Rindes auf Gesundheit und Wachstum verschiedener Organismen,

Biol. Zentralb., XLII, 109-112.
Hogben, Lancelot T., 1927: ''The Comparative Physiology of Internal

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Reactions of frog's melanophores to pituitary extracts, Proc. Roy. Soc.

London, Ser. B, XCIII, 318-329.
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Amphibia as effected by thyroidectomy, Jour. Exp. Zool., XXIX, 1-70.

9 pi.

Houssay, B. A., and L. Giusti, 1929: Le fonction de l'hypophyse et de la
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, L. Giusti, and J. M. Lascano-Gonzalez, 1929: Hypophysentrans-

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V, 397-418.

Humphrey, R. R., 1925: The development of the temporary sexual charac-
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testis, Anat. Rec, XXIX, 362.

Huxley, J. S., and J. F. Fulton, 1924: The influence of temperature on
the activity of insulin, Nature, CXIII, 234-235.

Ingram, W. R., 1929: Studies on amphibian neoteny; I, The metamorphosis
of the Colorado axolotl by injection of inorganic iodine, Physiol. Zool.,
II, 149-156.

Kendall, E. C, 1918: The active constituent of the thyroid, Jour. Amer.

Med. Ass., LXXI, 871.
Kleine, August, 1929: tiber die Parietalorgane bei einheimischen und

auslandischen Anuren, Jena. Zeitschr., XLXIV, 339-376.
Krogh, A., 1926: The pituitary (posterior lobe) principle in circulating

blood, Jour. Pharm. and Exp. Therap., XXIX, 177-189.
Larson, Mary Elizabeth, 1927: The extirpation of the thyroid gland and

its effects upon the hypophysis in Bufo americanus and Rana pipiens,

Sci. Bull. Univ. Kansas, XVII, 319-330, 2 pis.
Lascano-Gonzalez, J. M., 1929: Le destruction des surrenales chez le

crapaud, Bufo marinus (L) Schneid., Compt. rend. Soc. Biol., CII,

458-459.

Martin, E. G., and R. B. Armistead, 1922: The influence of adrenalin on
metabolism in various excised tissues, Amer. Jour. Physiol., LXII,
488-495.

Marx, L., 1929: Entwicklung und Ausbildung des Farbenkleides beim
Feuersalamander nach Verlust der Hypophyse, Arch. Entw. Mech.,
CXIV, 512-548.

Maurer, F., 1906: Die Entwickelung des Darmsystems, Hertwig's Handb.
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THE BIOLOGY OF THE AMPHIBIA

McCord, C. P., and F. P. Allen, 1921: Evidence associating pineal gland
function with alteration in pigmentation, Jour. Exp. Zool., XXIII,
207-224.

Nakamura, T., 1927: Etude anatomo-comparative embryologique et
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Noble, G. K., 1924: The "retrograde metamorphosis" of the Sirenidae;
Experiments on the functional activity of the thyroid of the perenni-
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, 1929: Further observations on the life-history of the newt, Triturus

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, and S. H. Pope, 1929: The modification of the cloaca and teeth of

the adult salamander, Desmognathus, by testicular transplants and
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Patch, E. M., 1927: Biometric studies upon development and growth in
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Soc. Physiol. Hist. Nat. Geneve, XL, 150-152.
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THE BIOLOGY OF THE AMPHIBIA

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Wochenschr., II, 1344-1346.

CHAPTER XIV

THE SENSE ORGANS AND THEIR FUNCTIONS

The sense organs are the receptors, either cells or more usually
groups of cells, which respond to environmental changes. The
resulting excitation is transmitted by means of nerves to effector
organs which may bring the animal closer to some particular need
or away from danger. Sense organs are usually formed of
epidermal cells. They are especially sensitive to only one par-
ticular kind of stimulus, and are far more sensitive to this than
are other cells of the body. A tactile papilla in the skin of a frog,
for example, is more sensitive to a slight touch than is the nerve
leading away from this spot. The kind of sensation produced
by a sense organ is not dependent on the type of receptor but on
the connections of the nerve in the brain or spinal cord. It
is known in man that the same sensation is produced by stimu-
lating either the sense organ or its nerve alone and hence that the
receptor is not responsible for the quality of a sensation. The
central connections are so different in frog and man that it would
be difficult to postulate the qualities of the sensations of the
former. Further, Amphibia are equipped with some sense organs
not found in man. The skin, for example, is sensitive to light
but there is little evidence as to the nature of the sensation which
comes from light-exposed skin. Many reactions in Amphibia
are reflex, presumably without representation in consciousness,
and all may be discussed without reference to the probable
sensations.

Sense organs may, therefore, be more properly called "recep-
tors." They may be grouped according to the type of stimulation
to which they are especially sensitive. The mechanorecep-
tors respond to certain degrees of mechanical pressure or certain
frequencies of vibration. These include the pressure receptors
of the skin and internal organs, the lateral-line organs of the
skin, the gravity receptors of the inner ear, the sound receptors
of the same, as well as the hunger receptors of the stomach. The
chemoreceptors include the organs of taste, smell, and common

317

318

THE BIOLOGY OF THE AMPHIBIA

chemical sense. The photoreceptors are the light receptors of
eye and skin. The thermoreceptors are those especially sensitive
to slight changes of temperature and embrace the temperature
organs of the skin. In addition, there are pain receptors in both
the skin and some internal organs which cannot be classified
under any of these heads. For convenience of description the

sense organs may be grouped ac-
cording to their topographic
positions.

Lateral -line Organs. — The most
conspicuous sense organs of the
skin are the lateral-line organs.
These are little clusters of sense
cells usually forming shallow de-
pressions in the surface and ar-
ranged generally in definite rows
on head and body. The lateral-
line organs represent an inheri-
tance from the fishes in which the
same rows may be readily identi-
fied. As in fishes these sense cells
function in responding to vibra-
tions of low frequency (Dye, 1921)
in an aquatic medium. Lateral-
line organs are present in all
thoroughly aquatic urodeles and
their larvae. They are present in

showing nerve terminations about gome mountain-brook Species Such
the sense cells. {After Chezar.)

as the larger forms of Desmogna-
thus, but are inconspicuous or lacking in the more terrestrial
forms of the same genus. They are lacking in terrestrial
plethodontids. Although present in larvae of all Ambys-
toma, they show various stages of degeneration in the adults.
Among the Salientia lateral-line organs are present in the aquatic
larvae but usually are absent in the adults. They are found in
the adults of the Pipidae (Escher, 1925) and of such very aquatic
types as Bombina and Ceratophrys laevis.

The lateral-line organs of Amphibia are less specialized than
those of most fish in that they usually lie entirely within the epi-
dermis. In Stereochilus they have sunk partly into the corium and

Fig.
lateral

113. — Vertical section of a
line organ of Siren lacertina

THE SENSE ORGANS AND THEIR FUNCTIONS

319

are found at the bottom of conspicuous "pores" on the head and
body.

The lateral-line organs are pear-shaped with a shallow, usually
ovate depression at the smaller, outer end. The organ consists
of sense cells having a central position and of spindle-shaped,
sustentacular cells surrounding them (Fig. 113). Charipper
(1928) also distinguishes mantle or protective cells on the sides
of the organ and basal cells next to the corium. The sense cells
are club-shaped and have a refractive point or bristle which is
proportionately longer in the larva than in the adult (Kingsbury,
1895) but in both cases reaches the surface of the depression where
it projects into the medium of the environment.

In some tadpoles and urodeles the lateral-line organs are
arranged singly in rows. In many others the organs divide to
form many short series of from two to seven organs with the axis
of each group either parallel or vertical to the main rows (Fig.
114). Kingsbury and Escher recognize four main rows on the
head and three on either side of the body. One of the head rows,
namely that on the cheek, may be conveniently divided into five
differently directed parts. The Pipidae differ from urodeles in
having an accessory row of lateral-line organs extending to near
the midline of the back and in having the supraorbital row
recurving and extending back into the frontal region. Salientia,
also, differ from urodeles, except Ambystoma, in having the axes
of the sense-organ groups of the upper body row extending in the
same direction as this row, those of the two lower rows running
vertical to it. The opposite arrangement of organ groups and
body rows is maintained generally in urodeles. In some Amphibia
the sense-organ groups on the head may be very numerous and
somewhat irregular but nevertheless are referable to the same
row patterns found in other recent species and in fossil Amphibia
and fishes.

These rows are determined by the lateral-line nerves of which
there is a preauditory component from the seventh cranial nerve
and a postauditory component from the ninth and tenth. The
three rows of lateral-line organs on each side of the body are
supplied by three branches from the latter. The central connec-
tion of both lateral-line nerves is in the dorsal portion of the
medulla. This suggests a close functional relationship of the
lateral-line organs with the mechanisms of equilibrium and
posture.

320

THE BIOLOGY OF THE AMPHIBIA

Lateral-line organs are readily lost when Amphibia become
terrestrial. The common newt possesses a full equipment
of these sense organs as a larva but during the terrestrial
red eft stage they partially atrophy and are covered by
adjacent epidermis to reappear again on the surface as fully
functional structures when the newt takes up an aquatic mode of

Fig. 114. — Lateral-line organs. The distribution of the lateral-line organs
is indicated by small depressions in the skin. A. Pleurodeles waltl (after Escher)-
B. Triturus viridescens (after Kingsbury). C. Rana heckscheri tadpole.

Branches: A., angular; D., dorsal; I.O. , infra-orbital; J., jugular; L., lateral;
O., oral; V., ventral; S.O., supra-orbital.

living in adult life. Nevertheless, lateral-line organs are not
present in all aquatic Amphibia, and here the immediate history
of any one form may be of great significance. Thus they are not
present in the aquatic toads Pseudis or Calyptocephalus nor in the
caecilian Typhlonectes (Escher, 1925). The latter, although
thoroughly aquatic, probably had fossorial ancestors. They
are found in the larvae of Salamandra atra which live their whole

THE SENSE ORGANS AND THEIR FUNCTIONS 321

larval life within the maternal oviducts (Escher, 1925). This
seems to be an inheritance from the ancestral Salamandra sala-
mandra which has aquatic larvae.

Tactile Organs. — The skin of Amphibia is sensitive to mechani-
cal stimulations. Free nerve endings are abundant between the
cells of the epidermis. Other nerve endings are associated with
connective tissue capsules or with groups of specialized cells
between which the nerves extend. When such groups occur in
the corium they may raise the overlying epidermis into a papilla.
Sense papillae have been described from the feet of frogs and
from the back of the breeding female frog. Papillae having a
similar form are found on the heads of some Salientia (Fig.
34B) and along the lips of some species of Desmognathus. The
tentacle of the Gymnophiona is a tactile organ, and the tentacles
of Xenopus larvae, as well as the cirri of certain plethodontids,
may have similar functions. The tentacles of the adult Xenopus
are not homologous with those of the larvae. They develop
by a growth of the caudal ends of the lacrimal ducts and their
function has not been determined.

Organs of Chemical Sense. — The outer surface of most fishes
is open to chemical stimulations of a mildly irritating kind
(Parker, 1922). With the development of land life in tetrapods
and the consequent drying of the skin this capacity was restricted
to the mucous membranes. The Amphibia still retain the
common chemical sense in a marked degree over all the surfaces
of their body. Free nerve endings of the spinal and cranial
nerves in the epidermis are the type of nerve terminals concerned
with the reception of chemical irritants. These receptors
resemble those concerned with pain, but Crozier (1916) has
shown that in the frog the same terminals do not function for
both mechanical and chemical stimulations. Further, Sayle
(1916) finds that fatigue resulting from chemical stimulation is
different from that produced by mechanical stimulation. The
presence of a delicate chemical sense in Amphibia would doubtless
play a part in affecting their movements in nature. Stimulation
of these sense organs would tend to induce avoiding or escape
reactions. In this they would be distinguished from olfactory
sensations which frequently induce approach reactions. The
olfactory organs are the chief receptors for chemical stimulations
in higher vertebrates and even in Amphibia they are more sensi-
tive than the chemical sense organs of the skin.

322

THE BIOLOGY OF THE AMPHIBIA

Heat and Cold Receptors. — Amphibia are sensitive to changes
in temperature. This has been well shown by Wright (1914)
and others who have recorded the temperatures at which different
species of frogs appear from their winter quarters. It has been
assumed that free nerve endings in the epidermis are the cold
receptors (Plate, 1924). Morgan (1922) noted that the reaction
time of frogs was longer to heat than to cold stimulation and
concluded that the heat receptors lay deeper in the skin. By
treatment with cocaine Morgan eliminated the response to cold
earlier than that to pain stimulation. The result suggests that
the heat and cold receptors are different from pain receptors.

After cocainizing the skin a re-
sponse to acid and to pain per-
sisted beyond the response to
heat, and the response to heat
and cold beyond that to touch.
Therefore the receptors for acid,
heat, cold, pain, and touch in the
skin of the frog are probably
different.

Organs of Taste. — Although
many fishes, such as the catfish,
have taste buds over the entire
outer surface of the body, these
structures, and with them the
sense of taste, became limited in
the Amphibia to the mouth. The senses of smell and taste are
closely allied physiologically but the organs are very different
structurally. Taste buds are isolated groups of elongated cells
widely distributed over the palate, jaws, and tongue (Fig. 115).
The groups on the palate of urodele larvae are smaller than those
of the tongue of adult frogs, and it has been suggested that these
groups of sense organs in the frog may be tactile instead of
gustatory organs. They consist of cylindrical as well as elongate
cells (Niemack, 1893), both of which lack cilia, in contrast to
most of the lining cells of the mouth. On the tongue of the frog
the taste buds occupy the summits of fungiform papillae which
are scattered among the filiform papillae and with them form the
plushlike surface of the organ. There are no separate gustatory
nerves as there are olfactory nerves, but gustatory fibers are
included in several cranial nerves, apparently in the fifth, seventh,

Fig. 115. — Taste bud from the
tongue of Necturus maculosus. Cor.,
corium of close connective tissue; Ep.,
epithelium; S.O., sensory organ
situated on a papilla of connective
tissue. (After Kingsbury.)

THE SENSE ORGANS AND THEIR FUNCTIONS 323

ninth, and tenth. The taste buds are sometimes encircled by
dense spirals of nerve fibers which may possibly reenforce the
sensory excitation of these organs (Herrick, 1925). In man
different taste buds may be responsible for different taste quali-
ties. The Giersbergs (1926) have shown that the same is prob-
ably true for Amphibia.

Olfactory Organs. — The organ of smell, which in most fishes
lies with both inlet and outlet on the surface of the snout,
became associated with the upper lip in the fish ancestors of
tetrapods and had its outlet enclosed within the mouth in these
forms. Caecilians and some other Amphibia (Kurepina, 1926,
1927) show in their development how this was apparently
accomplished in phylogeny, for the choanae or internal nares
arise from the caudal end of a furrow, the oro-nasal groove
(Fig. 11), which sinks within the developing upper lip.

Some aquatic Amphibia, especially the perennibranchs, agree
with the fishes in that the nasal chamber is lined with a series of
folds. The depressions between the folds are clothed with sense
cells, and the ridges are covered with ciliated respiratory epi-
thelium. Larval urodeles in general have a discontinuous
sensory area, while tadpoles and most metamorphosed Amphibia
have an undivided one. In Salientia this is raised caudally into
an eminentia olfactoria.

The olfactory epithelium consists of sense cells bearing several
olfactory hairs on their free ends. It also includes ciliated
supporting cells and basal cells. In tadpoles and larval urodeles
the ciliated cells beat rapidly and help to drive a current through
the nasal chamber. Wilder (1925) showed that in a plethodontid
larva these cilia, together with those on the gills, maintained a
steady current entering the nasal chamber. The sense cells
vary greatly in length (Fig. 116), and in Rana some of the hairs
may be longer than the thickness of the epithelium (Hopkins,
1926). The proximal end of each sense cell is drawn out into a
fine process.

Two glandular masses develop in association with the nasal
passage in metamorphosed Amphibia: an outer, guarding the
external nares, and a more extensive inner series, which keeps the
olfactory epithelium moist (Fig. 117). The secretion of the latter
forms a mucous layer over the olfactory surfaces in those urodeles
and Salientia which take air into the nasal chamber. Many
olfactory hairs penetrate this layer and lie with their distal

324

THE BIOLOGY OF THE AMPHIBIA

portions exposed to the air (Hopkins, 1926). In thoroughly
aquatic forms the mucus does not form a layer and the hairs
stand out in the water in the nasal passage. Thus, in neither
case does the mucus form a medium in which odorous substances
are dissolved before they stimulate the hairs.

The olfactory hairs of Amphibia are functional both in an air
and in a water medium, as has been well shown in the case of the
newt (Matthes, 1926). The olfactory organ, however, reaches
its highest state of development in terrestrial forms. In the
larvae of frogs and salamanders the olfactory stream passes

Fig. 116. — Diagram of the olfactory epithelium of a frog. The long hairs
reach the surface of the mucus and are non-moving. The shorter ones fail to
reach this surface and exhibit ciliary activity. O.Ep., olfactory epithelium;
L.O.H., long, non-moving, olfactory hairs; M.L.S., surface of mucous layer;
S.O.H., short, moving, olfactory hairs. (After Hopkins.)

freely inward from the nasal cavity to the mouth. Its return
to the nasal passage is prevented in urodele larvae by a simple
flap of mucosa acting as a valve, while in tadpoles a double fold
or fringe has a more complex form but similar function. During
metamorphosis the choanal valves are lost and a new mechanism
for closing the nasal passage appears at its other end. As shown
by Bruner (1901, 1914), a constrictor and two dilators of the
external nares develop at this time or shortly before the choanal
valves are lost. In metamorphosed Amphibia the olfactory
stream under muscular control passes freely in and out through
the nasal cavity. The inspired stream tends to move through

THE SENSE ORGANS AND THEIR FUNCTIONS

325

the mesial part of the nasal chamber; the expired, through the
lateral. The latter region becomes more or less devoid of olfac-
tory epithelium, except at one point, where a special sense area
develops. This is Jacobson's organ (Fig. 117), and it serves to
test the food substances in the mouth. In frogs Jacobson's
organ lies in a sac at the anterior mesial corner of the nasal
chamber. In urodeles it has usually a lateral position which,
in spite of the studies of Wilder (1892), Seydel (1895), and Anton
(1908), has caused various investigators to doubt its homology

Fig. 117. — Cross-section of nasal cavity of a tree frog showing Jacobson's
organ and the glands associated with the nasal cavity. CP., cartilago para-
nasals; C.P.I. , cartilago paraseptalis inferior; C.P.S., cartilago paraseptalis
superior; C.S., cartilago septi; D.J., recessus medialis nasi (ductus Jacobsoni) ;
D.N., ductus nasolacrimal; D.Ol., ductus olfactorius; Gl.J., glandula Jacobsoni;
Gl.N.L., glandula nasalis lateralis; Gl.P., glandula palacinus; Mx., maxilla;
Os.N., os nasale; P. I., pars intermedia; R.M., recessus maxillaris. (After
Mihalkovics.)

with the mouth tester of frogs. The perennibranchs present
certain deviations from the larval condition. Siren and Amphi-
uma have both developed a modification of the choanal valve
which permits its being opened at will (Bruner, 1914a), and both
forms which are terrestrial at times, have a well-developed Jacob-
son's organ. Cryptobranchus, which represents a partly meta-
morphosed type, has lost the choanal valves and developed a
Jacobson's organ. This structure arises in the larvae in anticipa-
tion of its use after metamorphosis, and hence it is not surprising
to find that Siren and Amphiuina with their special valves have

326

THE BIOLOGY OF THE AMPHIBIA

elaborated this structure while Necturus and Proteus which
retain the larval valves have failed to develop it. It is interesting
that Megalobatrachus should have its Jacobson's organ pro-
portionately larger in early life than later (Fleissig, 1909). This
would confirm the conclusion that the structure first developed
in connection with terrestrialism and that its elaboration in
Siren and Amphiuma is correlated with their occasional excur-
sions on land. The olfactory nerve fibers extending to Jacobson's
organ frequently form a bundle distinct from those connecting
with the remainder of the nasal chamber.

Caecilians apparently sprang from a different order of extinct
Amphibia from that which gave rise to the frogs and sala-
manders, and they are unique in possessing a short retractile
tentacle on either side of the face. Its base becomes associated
with the nasal passage and especially with a secondary olfactory
area usually described as Jacobson's organ. By movements of
the tentacle, odorous substances are apparently brought in
contact with this sensory region, and hence Laubmann (1927)
describes the region as a tactile nose able to detect food inde-
pendently of the respiratory stream. The great development of
the olfactory region in caecilians is correlated with their burrow-
ing habits and rudimentary eyes.

Eyes. — The first tetrapods were confronted with the problem
of modifying the shortsighted fish eye into a mechanism better
adapted for vision in the air. Amphibia have a smaller lens than
fish, and it lies behind the iris. It is not round except in certain
larval forms but flattened on its outer surface, even in the primi-
tive hynobiid salamanders (Okajima, 1910). In frogs and
toads this flattening is carried farther than in urodeles. The
retreat of the lens away from the cornea, as well as its flattening,
would tend to make the amphibian eye farsighted, an advanta-
geous condition not realizable in water because of the opacity of
this medium. The eye in its new environment required at the
outset protective lids and glands to keep it clean and moist.
Special muscles of accommodation developed to increase the effi-
ciency of focus, and as the first tetrapods were devoid of necks,
other muscles were modified to periscope the eyeball above the
surface of the head and to pull it down when it was in danger of
injury. The eyes of Amphibia are of interest in that they show
stages in the transition from the eyes of fish to those of higher
vertebrates

THE SENSE ORGANS AND THEIR FUNCTIONS

327

The eyes of modern Amphibia vary enormously in size.
Arboreal and terrestrial forms tend to have larger ones than
fossorial or aquatic types. The eyes are directed laterally in
most forms, but in Centrolenella, Zachaenus, and a few other
Salientia they are directed partly forward and possibly effect a
binocular vision. Verrier (1927) estimated that even in the
European tree frog 40 per cent of the field of vision was binocular.

The eyeball is covered distally by a transparent cellular mem-
brane, the cornea, the remainder, or concealed portions, being
protected by a dense fibrous coat, the sclera. The latter is
strengthened in the adults of some primitive urodeles, as well as
in the larvae of most forms, by a ring or cup of cartilage (Stadt-

A B

Fig. 118. — Sections representing three stages in the development of the eye
of the frog, Rand esculenta. A.L., anlage of lens; Br., brain; Ep., epidermis;
L., lens; O.C., optic cup. (After Giesbrecht.)

muller, 1914; Okajima and Tsusaki, 1921). This cartilage, which
is also found in frogs, was partly ossified at least, in some of the
first tetrapods. It becomes enormously thick in Cryptobranchus,
where Plate (1924) considers it a case of disharmonic growth
conditioned by the degeneration of the eyes of this form. The
cornea is arched in metamorphosed Amphibia and due to the
inward migration of the lens (Fig. 118) is part of the refractive
system. The cornea of larval Amphibia is frequently double, as
in the case of certain bottom-living fish. The inner cornea arises
from subcutaneous tissues and later fuses with the outer on
metamorphosis (Giesbrecht, 1925).

The eyelids first develop at metamorphosis. They are reduced
in some aquatic Salientia and entirely absent in two genera of

328 THE BIOLOGY OF THE AMPHIBIA

pipid toads. The upper eyelid of Amphibia is merely a thick
fold of integument incapable of independent movement. The
lower eyelid undergoes various modifications within the group.
In some urodeles, such as Hydromantes italicus, the lower eyelid
lacks muscles, but in others, as Triturus, strands from the M.
periorbita penetrate the temporal and nasal sections of its upper
edge (Franz, 1924). The upper portion of the lower lid is thinned
and slightly folded on itself in our common newt. The folding is
carried further in the primitive Salientia until finally, in Rana and
many other frogs, it is a thin, translucent membrane which
folds inside the thicker lower part, the whole structure being
N-shaped in cross-section. The upper part is called the " nicti-
tating membrane," although it seems to have arisen wholly within
the Amphibia. It is possibly homologous with the nictitating
membrane of other vertebrates, however. It arises during
ontogeny from a small mass of undifferentiated tissue embedded
within the integument at the anterior border of the tadpole eye.
Lindeman (1929) has shown that the extirpation of this mass
prevents the nictitating membrane from forming during metamor-
phosis, while the removal of the ventral border of the eye results
in its partial regeneration and a perfect nictitating membrane
being formed. Hence the anterior mass of tissue appears to be
alone responsible for the development of the nictitating mem-
brane. In a few tree frogs both parts of the lower lid are trans-
lucent or even transparent. The so-called nictitating membrane
has attached to either end of its thicker upper margin a tendon
which encircles the greater part of the eyeball. When the eyeball
is retracted within the orbit, the nictitating membrane by the
pull of the tendon is automatically drawn up over the cornea.
It is folded again partly by the protrusion of the eyeball but
chiefly by the contraction of a special muscle which arises from
the levator bulbi.

Correlated with the development of lids, eye glands made their
appearance for the first time in the Amphibia. Primitively in the
group a single gland is found extending the length of the lower
eyelid and opening by numerous ducts on the conjunctiva.
This condition is found in most Caudata. In Salamandra the
gland is partly divided into two heads: an anterior Harderian
and a posterior lacrimal mass characteristic of the higher verte-
brates. In the Salientia only the anterior of these two glands
is retained. In the Gymnophiona a single enormously hyper-

THE SENSE ORGANS AND THEIR FUNCTIONS 329

trophied gland is present occupying the whole eye socket and
functioning to lubricate the tentacle. Developmental studies
have shown this gland to arise from the same region as the eye
gland of urodeles and to be homologous with it.

The secretion of the eye glands is conducted to the nasal
chamber by the lacrimal duct. In urodeles it opens on the con-
junctiva near the inner corner of the eye, while in the Salientia it
usually opens in the middle of the lower lid. Recently metamor-
phosed Salientia (Piersol, 1887) and certain primitive Caudata
(Okajima, 1910) may have the duct opening on the surface of
the skin near the inner corner of the eye. This seems to be the
original position of the mouth of the lacrimal duct in Gymno-
phiona. Lids, eye glands, and lacrimal duct are formed during
or just before metamorphosis. Their complete absence in the
perennibranchs is due to the failure of these forms to metamor-
phose rather than to any secondary degeneration, as many writers
assume.

The eyes of many Amphibia, particularly the tree frogs, are
very beautiful, for the iris, often vividly marked with gold or
red, is clearly visible through the transparent cornea. Some
of this pigment is found not in pigment cells but in the smooth
muscles which bring about a rapid contraction or expansion of the
iris under the direct action of light. The sphincters lie near the
aperture in the iris, while the dilators extend radially and lie more
laterally. The aperture, the pupil, varies greatly in form
throughout the Amphibia and has been used by systematists in
denning natural groups of Salientia. It is horizontal in most
frogs and toads, vertical in the Spadefoot Toads, while in certain
genera of discoglossids and Hylidae it may be three- or four-
cornered.

Accommodation. — The eyes of Amphibia are of considerable
phylogenetic interest in that the mechanism of accommodation
is intermediate between that of fish and Amniota. The lens lies
behind the iris and is held in place by a series of delicate radiating
fibers which extend from the outer margin of the lens to the ciliary
body, a vasculated fold of the inner coat of the eye capsule. The
eye at rest is moderately farsighted. Accommodation is accom-
plished not by a change in the form of the lens as in Amniota but
by a change of its position as in fishes. In frogs a dorsal and
ventral protractor lentis (Fig. 119) is present in the ciliary fold.
Its contraction moves the lens outward, not inward as does the

330

THE BIOLOGY OF THE AMPHIBIA

lens muscle of fishes. In urodeles there is only a single ventral
muscle lying in a papilla. This functions the same as the ventral
protractor of frogs and is considered by Tretjakoff (1906) to be
homologous with it. The urodele protractor is believed by Plate
(1924) to be homologous with the fish retractor, and hence the
Amphibia may owe this system to their piscine ancestors. In

all Amphibia there is a second
muscular system which is not
found in fish. This is the
tensor chorioideae, a series of
meridionally arranged fibers in
the periphery of the ciliary
region. Streuli (1925)
believes this functions antag-
onistically to the protractor,
but Beer (1899) and Plate
(1924) present evidence to
show that it functions in mov-
ing the lens in the same direc-
tion. The tensor chorioideae
becomes the ciliary muscle of
the eye in amniotes (Plate,
1924).

The extent of accommoda-
tion varies with the species
but shows some correlation
with the species habits. It is
apparently greatest in the ter-
restrial Bufo and least in such
aquatic forms as Bombina.
Newts have been reported to be nearsighted on land but not in
the water.

Retina. — The eye is fundamentally unlike other sense organs
in that the retina is not directly evolved from the external ecto-
derm but from part of the central nervous system. It arose in
phylogeny from an aggregation of direction eyes (Parker, 1908)
which were inverted on the development of a tubelike central
nervous system. Thus the rods and cones, the only photosensitive
cells in the eye, are directed away from the lens and light passes
through several layers of nerve fibers and their nuclei as well as
much supporting tissue before reaching the sensitive cells.

Fig. 119. — Vertical meridian section
of a frog's eye, showing muscles of
accommodation. C, cornea; iris;
L., lens; M.P.L., M. protractor lentis;
M.T.C., M. tensor chorioideae; P.C.R.,
pars ciliaris retinae; R., retina; R.V.,
ring vessel; Z.C., zonula ciliaris. {After
Tretjakoff.)

THE SENSE ORGANS AND THEIR FUNCTIONS 331

Between lens and the innermost of the retinal layers is a solid
mass of transparent connective tissue, the vitreous humor. This is
penetrated by a network of fibers and blood vessels and covered
by a thin membrane in the frogs. In the urodeles the fibrous
material is less developed. The outer chamber of the eye, that
between cornea and lens, is filled by a watery fluid, the aqueous
humor.

The retina consists of an outer pigmented epithelium against
which the rods and cones abut. The nuclei of the rods and cones
form a layer immediately central to them. Their axons do not
connect directly with the optic nerve, but two successive layers
of neurons are intercalated. The eye is the only sense organ
which contains such connecting neurons within its limits. The
rods are of two kinds in Rana : red with a long, and green with a
short outer segment. The latter type of rod is lacking in Nec-
turus, Salamandra, and various other urodeles. Rods of the
former type owe their color to the visual purple which quickly
bleaches in light, the products of this decomposition inducing an
excitation in the rods. The visual green is allied to visual purple
and has the same function. Cones are smaller than the rods and
less numerous. They are believed to function in color vision,
different cones being stimulated by light of different wave lengths.
Form perception is accomplished by the stimulation of both rods
and cones in the different parts of the retina.

Rods and cones consist chemically and physically of two
parts, the outer and inner segments (Fig. 120). The outer
segment, which is strongly refractive, is in the form of a cylinder
in the rods and of a peaked cap in the cones. The inner segment
is characterized in frogs and toads by a planoparabolic lenslike
structure. In urodeles there are present two lenslike bodies,
a proximal biconvex body, fitting into a distal planoconcave
body, the ellipsoid. Further differentiations have been recorded
in the rods and cones of Amphibia (for review see Arey, 1928).
The cones contract on exposure to light, even when not fully
differentiated (Detwiler, 1923). Double cones are regularly
present in the eyes of various urodeles, and as the members of
each pair differ in size, they probably have different functions.
The eyes of salamanders function not only during development
but apparently also during degeneracy. Those of cave sala-
manders having a very degenerate retina may be sensitive to light.
Dubois (1890) found that while the skin of Proteus is very sensi-

332

THE BIOLOGY OF THE AMPHIBIA

tive to light, the latent period of reaction was more than doubled
by covering the vestigial eyes with lamp black. On the other
hand, Obreshkove (1921) concluded that the well-developed
eyes in the tadpoles of Rana clamitans played no part in the
responses of the tadpoles to light. Probably under other con-
ditions of illumination the eyes would have important functions.

Rods and cones are evenly distributed over the retina of Nec-
turus (Palmer, 1912), but in Rana a thickened portion of the
retina seems to mark a region of acute vision since cones are
especially abundant here. Chievitz (1889) reports two species
of Bufo as having a shallow depression in this region, an incipient

Fig. 120. — Visual cells of a salamander. The rods and cones from the retina
of a larval Ambystoma. Bic.B., paraboloid; C.N., cone nucleus; D.C., double
cone; EL, ellipsoid; O.S.C., outer segment of cone; O.S.R., outer segment of rod;
R.N„ rod nucleus. (After Detwiler and Laurens.)

fovea developed in species known to have a better vision than
Rana.

Keenness of vision is dependent not only on a focusing of the
lens in such a way that a clear image is thrown on the retina but
also on proper illumination of the retina. In strong light the
iris rapidly contracts and the pigment cells in the retina send out
processes which cut down the amount of light reaching the rods
and cones. The dark-adapted eye of the frog exhibits not only a
contraction of the pigment cells but a rod contraction and a cone
elongation. The pigment contraction is, however, influenced by
temperature. Less contraction is found to accompany exposures
at high temperatures than at low temperatures in the dark
(Detwiler and Lewis, 1926).

THE SENSE ORGANS AND THEIR FUNCTIONS

333

Some species of Amphibia are diurnal, but their retinas have
not been investigated to determine whether they differ from those
of nocturnal relatives. It may be noted, however, that some
forms, such as Necturus and Gyrinophilus, which are primarily
if not entirely nocturnal, possess both rods and cones. A few
frogs have an appendage from both the upper and lower margins
of the pupil. Its chief function would seem to be secretory and
not the masking of light from the retina.

Degeneration of the Eye. — In addition to the usual six eye
muscles of vertebrates, the Amphibia possess a special retractor
bulbi, which pulls the eyeball within the orbit, and a levator bulbi,
which raises the eyeball again. In blind vertebrates the eye
muscles frequently degenerate. In caecilians the typical eye
musculature has been modified by the degeneration of some
muscles and nerves and by the transfer of others to adjacent
regions where they have different functions. The retractor bulbi,
is transformed into a retractor tentaculi; the rectus internus, into a
retractor of the tentacular sheath; and the levator bulbi, into
compressor and dilator muscles of the orbital glands (Norris,
1917).

In addition to most burrowing Gymnophiona, which exhibit
various stages in the degeneration of the eyes, there are three
other Amphibia, species of salamanders, all inhabitants of caves,
which are blind in the adult stage. The European Proteus has
been most extensively studied. Its eye is essentially a case
of arrested development (Schlampp, 1892; Kohl, 1895), although
certain degenerative changes have occurred. The American
Typhlomolge exhibits further degenerative changes. The eye
muscles and lens have vanished; retina and vitreal cavity are
greatly modified. Probably in Typhlomolge, as in Typhlotriton
and Proteus, the eye develops normally until a certain stage when
growth is checked, differentiation ceases, and degenerative changes
arise.

Ears. — The most primitive embolomerous Amphibia swam in
the aquatic medium of their fish ancestors and were equipped with
an ear apparatus only slightly different from that of fish. With
the development of land life the gill pocket between mandible
and hyoid no longer broke through to the outside as a spiracle,
but its end abutted against the integument in the spiracular region.
The integument of this spiracular region became, then, thinned.
The resulting drum head, or tympanum, characterizes most

334

THE BIOLOGY OF THE AMPHIBIA

Salientia, although a few have the integument unmodified
and separable from the underlying drum, and many burrow-
ing or aquatic types as well as all the urodeles lack both drum and
middle ear. This might be considered evidence that the urodeles
sprang from aquatic or burrowing ancestors. Amphibia were
primitively equipped with a tympanum which was fully exposed
on the side of the head. It is curious that in one frog (Rana
cavitympanum of Siam), the tympanum has sunk below the
surface and lies at the end of an external ear opening as in
mammals.

In the first land vertebrates as well as in their immediate
ancestors, the support of the lower jaw was shifted from the

Fig. 121. — Diagram of the sound transmitting apparatus of an aquatic larval
(A) and a terrestrial adult salamander (B). Col., columella; F.V., fenestra
vestibuli; H.A., hyoid arch; L.S-C, ligamentum squamoso-columellare; M.L.,
skeleton of the lower jaw; M.Op., musculus opercularis; Op., operculum; Pq.,
palatoquadratum; Sq., os squamosum; S.S., suprascapula ; St.C, stilus columellae.
(After Kingsbury and Reed.)

hyomandibular to the quadrate. The freed element sank into
the spiracular cavity and assumed a new function of transmitting
sound vibrations from the tympanum to the ear capsule. In
Eogirinus, this hyomandibular, now called a " columella,"
merely abutted against the ear capsule, but very early in laby-
rinthodont phylogeny a fenestra was formed which increased the
efficiency of transmitting vibrations to the perilymph, the fluid
surrounding the membranous labyrinth or inner ear.

Modern Amphibia show in their ear apparatus some evidence
of terrestrial ancestry. In addition to the columella which
has its platelike proximal end fitting into the fenestra vestibuli,
there is present primitively in both frogs and urodeles a second
bony or cartilaginous plate in the same fenestra. This element,

THE SENSE ORGANS AND THEIR FUNCTIONS

335

the operculum, is primitively not attached to the columella but
is equipped with a muscle which attaches to the shoulder girdle
and serves to transmit vibrations from the ground via the forelegs
to the perilymph (Fig. 121). The operculum usually develops
first at metamorphosis and is, therefore, absent not only in
larvae but also in most of the perennibranchs. In Amphiuma
and Necturus (Reed, 1920) it is present but fused to the columella.
In aquatic Amphibia the operculum and its muscle would be
practically functionless. Hence, it is not surprising to find
operculum and columella fused in Pipa. In metamorphosed
urodeles of the more advanced families, the columella undergoes
various modes of degeneration, any one mode being usually
found throughout a natural group of genera (Reed, 1920; Dunn>
1922).

The loss of the outer and middle ear in burrowing toads such
as Pelobates does not seem to inconvenience them during the
breeding season, for the loud calls of the males would be readily
transmitted through the water in which the sexes congregate
during the breeding season. The degeneration of the Eustachian
tube in Bombina and Pelobates has not gone so far as it has in
the urodeles. Both possess a tube (Litzelmann, 1923), but it
never widens out to form a middle ear. The rudimentary ear
ossicles and the absence of Eustachian tubes in Ascaphus would
seem to be correlated with a mountain-brook life where acoustic
conditions are obviously bad. Ascaphus, however, apparently
lacks a voice entirely.

Inner Ear. — The inner ear in all vertebrates is primarily an
organ of equilibrium. In fishes this organ is also able to detect
certain vibrations. With the development of land life in the
Amphibia, a special organ of hearing is evolved out of part of it.
The inner ear, being fundamentally a part of the lateral-line
system, arises as a placode on either side of the hind brain.
It forms a vesicle and, propelled by not clearly understood factors
(Streeter, 1921), leaves the skin and migrates to its final position.
There it eventually becomes surrounded by cartilage, which
is incorporated into the skull as the otic capsule. The vesicle
thins to form the membranous labyrinth and remains separated
from the otic capsule by a lymphlike fluid, the perilymph. The
labyrinth itself is not hollow but filled with a similar fluid. In
forming the labyrinth the vesicle becomes constricted into a
dorsal utriculus and a ventral sacculus. In some frogs the

336

THE BIOLOGY OF THE AMPHIBIA

sacculus may be constricted into a smaller upper and a larger
lower vesicle.

The utriculus gives rise to the semicircular canals which are
arranged in the three planes characteristic of all gnathostomes
(Fig. 122). The anterior and posterior canals are arranged
vertically and at an angle of 90 degrees to one another and 45
degrees to the median plane of the animal's body. The third
is at right angles to the other two and lies horizontally on their
outer side. The sacculus develops a small evagination, the
lagena, which is destined to form the cochlea of higher vertebrates.

Fig. 122. — Membranous labyrinth of the inner ear of M egalobatrachus japoni-
cus. The left labyrinth viewed from the outside. Amp. A., ampulla anterior;
Amp.L., ampulla lateralis; Amp.P., ampulla posterior; C.S.A., canalis semicircu-
laris anterior; C.S.L., canalis semicircularis lateralis; C.S.P., canalis semicircularis
posterior; D.End., ductus endolymphaticus; Lag., lagena; N.Ac., nervus acusti-
cus; P.Bas., pars basilaris; P.Neg., pars neglecta; R.Ut., recessus utriculi; Sac,
sacculus. (After Okajima.)

The sense organs arise from a common anlage which divides into
seven or eight areas. A patch of sense cells comes to lie at one
end of each of the semicircular canals. Each is covered by a
gelatinous cap, the cupula, and the canal at this point is swollen
into an ampulla. The utriculus becomes equipped with a macula
utriculi and a smaller m. neglecta (which is doubled in the caecili-
ans), the sacculus retains a macula sacculi and a papilla lagenae.
These four sense areas of the utriculus and the sacculus have
the sense cells extended into long processes over which lie a
gelatinous cover and in addition a layer of " hearing sand,"
crystals of calcium carbonate. Amphibia differ remarkably
from fish in possessing an additional sense area, the papilla
basilaris, which splits off from the papilla lagenae. It is covered

R. Ut.

C S. P.

Amp. P-

C S- U

THE SENSE ORGANS AND THEIR FUNCTIONS 337

L. P

H. C.

by a movable tectorial membrane (Fig. 123) and would seem to
serve as the chief organ of hearing. This organ is lacking in
many perennibranchs and is best developed in Salientia where
it lies in a small evagination of the lagena. A second hearing
organ of Salientia and of certain primitive urodeles including
Ambystoma (Norris, 1892) is the macula neglecta which in these
forms is also covered with a tectorial membrane.

The papilla basilaris alone of the sense areas was destined for
elaborate specialization in
phylogeny, for it alone has de-
veloped into the organ of sharp
hearing found in mammals and
birds. Plate (1924) suggests
that this may have been due to
its more favorable position near
the perilymphatic duct and
near a thin place in the sacculus
wall which would readily permit
the transference of vibrations s. c
from the perilymph to the
endolymph.

An advance of obscure func-
tional significance over the
conditions in the fish ear is
found in the perilymphatic duct.
This grows out from the mesial
wall of the sacculus and into the
brain cavity. In the Salientia
it forms with its mate a ring

around the hind brain, and continues posteriorly as an unpaired sac
along the spinal cord as far as the seventh vertebra. Its wall,
which may become partitioned by many septa, secretes a cal-
careous fluid which distends the sac to form a series of white
diverticula overlying the spinal ganglia. It has been said that
this enormous supply of calcium carbonate was utilized by grow-
ing bone, but Herter (1922) showed that tadpoles deprived of
these sacs grew as well as the controls. Possibly the vertebral
sacs transmit vibrations impinging on the back. They are lack-
ing in Bombina and Discoglossus, although present in most higher
Salientia, (Whiteside, 1922). The endolymphatic sacs of each
side may or may not fuse in the urodeles and the type of modifica-

Fig. 123. — Cross-section through
papilla basilaris of the newt, Triturus
cristatus. H., sensory hair; H.C., hair
cell; L.P., lamina propria; M.T., mem-
brana tectori; S.C., supporting cells.
(After Proebsting.)

338

THE BIOLOGY OF THE AMPHIBIA

tion agrees closely with the phylogenetic scheme (Dempster,
1930). The sacs never extend into the neural canal of the verte-
brae in urodeles, and this restriction is correlated with poorly
developed auditory powers in this group.

The several parts of the inner ear are supplied by branches of
the eighth cranial nerve. The sense areas are formed of two kinds
of cells: a flask-shaped sense cell, ending in a hairlike point, and a
narrower supporting cell. Sound vibrations are transmitted
through the ear ossicles to the perilymph which in turn transmits
the vibration to the membranous labyrinth including the tectorial
membranes overlying the two sense areas believed to be espe-
cially sensitive to sound waves.

Functions of the Ear. — The inner ear was originally an organ
of equilibrium, and in all vertebrates it has a very important
function to perform in this capacity. Tree frogs on swaying
limbs or salamanders in the swirl of mountain streams make
reflexly the proper movements to maintain their equilibrium.
The sense cells are stimulated when the animal is thrown to one
side or even when it is rotated slightly from a proper balance.
Compensatory movements of limbs, body muscles, and eyes are
automatically called forth by the nervous impulses initiated
from the stimulated sense cells.

There is still some uncertainty as to the specific functions of
each of the sense areas. McNally and Tait (1925) have pre-
sented evidence to show that in frogs the semicircular canals
detect quick or slow movements of direction in either a straight
or an angular course. Each vertical canal is associated with
the limb of that quarter of the body toward which it faces,
the anterior pair controlling the forelimbs and the posterior
pair the hind limbs. Stimulation of a vertical canal brings forth
an extension of the particular limb of that quarter. Stimulation
of a horizontal canal leads to a movement of at least two and
usually four limbs. Thus, the semicircular canals and their
associated nerves are mechanisms which prevent stumbling or
toppling over in any direction away from the normal position,
and they react with great speed in bringing about a compensatory
movement of the animal's limbs and body. The utricular macula,
on the other hand, is an organ of static equilibrium which notes
deviations from the normal direction of the pull of gravity. The
saccular macula is not in any way concerned with equilibrium

THE SENSE ORGANS AND THEIR FUNCTIONS 339

and hence would seem to play some part in recording sound
vibrations.

There have been many experiments on removing parts of the
inner ear and noting the effect on an animal's movements.
From these it is not clear that the utricular macula is the only
organ of static equilibrium (Pike, 1923; Fischer, 1926). The
different results may be due in part to injury to adjacent areas.
Removal of the whole ear brings about forced movements and
attitudes. The head and body are bent toward the operated
side (Greene and Laurens, 1922), and the legs of the opposite side
assume an extended and braced position. The ear is closely
associated with the tonus reflexes of the musculature, and some
of the movements it conditions are due to changes in these
reflexes. In the course of time, irregularities of locomotion
caused by the removal of one of the ears of tadpoles may be in
part corrected (Streeter, 1906). This would seem to be due to
learning to use the eyes as an aid to equilibrium. Herter (1921),
however, is of the opinion that the sense of touch may be utilized
by some tadpoles in learning to correct the locomotor disturbances
resulting from a loss of one labyrinth. Streeter found that if
both ear vesicles of the wood frog were removed at an early
stage of development, the tadpoles were never able to swim
effectively.

When frogs are rotated on a revolving table they make com-
pensatory movements with their heads. This may be due not
entirely to a stimulation of the labyrinth but also to visual
stimuli. Gruenberg (1907) arranged frogs in a stationary
position and revolved a cylinder of various figures and colors
about them. The frogs made compensatory movements similar
to those made when the table was rotated and the environment
was stationary. The response to the visual stimulus, however,
was relatively weaker and slower than that to the dynamic
stimulus of rotation. Thus, the labyrinth mechanism is the
chief organ of equilibrium whether or not it receives support
from the eyes.

Other Internal Mechanoreceptors. — The receptors which
induce a state of hunger in ourselves and which produce impulses
calling forth food-seeking reactions in frogs and other Amphibia
are located in the walls of the stomach and are stimulated
by hunger contractions of the empty stomach. No distinctive
types of receptors have been described from this region. Many

340

THE BIOLOGY OF THE AMPHIBIA

nerves send branched arborizations among the muscles, however,
and these apparently also serve as pressure receptors. Some
afferent nerves in various parts of the body end in bulbous end
organs in tendons and joints. Stimulations from these organs,
produced by pressure or pull of adjacent tissues during locomotion,
play an essential role in the coordination of bodily movements.

Dominant Senses. — A well-developed sense organ would be
considered good evidence that the sense in question played an
important part in the life of its owner. An examination of the
structure of the sense organs in Amphibia gives no clear evidence
as to which are the dominant senses. Experiments on common
forms, however, have shed some light on this question. Amphibia
may respond to stimulations in the laboratory which they never
receive in nature. If a weak electric current is passed through
an aquarium, tadpoles will swim or at least turn toward the
anode (Scheminsky, 1924) in the same automatic way moths
seek a flame. Most responses of Amphibia have a decided
utility, however, which may be considered together with the
response.

Smell, Taste, and Common Chemical Sense. — Food is detected
by most Amphibia chiefly by sight. It has been demonstrated
that some Amphibia are able to detect and to locate food by smell
alone (Copeland, 1913; Burr, 1916; Nicholas, 1922). Newts
which live both in and out of water are capable of smelling in
both media (Matthes, 1924). Newts approach and nose quies-
cent edible objects, and feeding reactions are elicited only if the
olfactory stimulations are adequate. Common toad tadpoles
react to olfactory stimulation, but adults make no response
(Risser, 1914). Although all toads are more or less crepuscular
and some are apparently nocturnal, Risser found that B. ameri-
canus would not eat food in the dark. Locher (1927) noted that
feeding reactions could be induced in Bufo calamita by motion-
less odorous objects, and hence within the genus Bufo, species
may vary in their olfactory abilities. No doubt burrowing
toads with well-developed olfactory organs must depend to a
large extent on odors in detecting their prey. The absence of
olfactory powers in some toads is surprising in view of the well-
developed "nose-brain" of these and other Amphibia. The
larvae, however, of toads and other Amphibia, have acute
olfactory powers. Apparently the sense of smell in most amphib-
ian larvae is of the same order if not so keen as that of fish.

THE SENSE ORGANS AND THEIR FUNCTIONS

341

This alone might account for the generous endowment of nose
brain.

The sense of taste is very closely allied to that of smell. The
amount of stimulating substance is, of course, usually greater
in the case of taste, and the central connections in the brain are
totally different. The response to the stimulation of a taste
bud in Amphibia is a snapping or swallowing reaction, while
that to an olfactory stimulation is a movement of head or body.
These different responses are due to the different connections
of sense organs with motor tracts in the two cases. The Giers-
bergs (1926) have shown that the European newts can distin-
guish various taste qualities. By cocainizing part of the nerve
endings in the tongue, they demonstrated that the tongue could
be made insensitive to quinine while remaining sensitive to salt
and acid. This suggests a certain specificity in the different
taste buds. Some tadpoles, such as those of the Wood Frog
and Spade-foot Toad, prefer meat to a vegetable diet. Obnox-
ious substances are often rejected by adult frogs. Still, adult
Amphibia are such indiscriminate feeders that they would seem
to have little need of a well-defined sense of taste.

The chief chemical sense which controls the general movements
of Amphibia is probably neither smell nor taste but a common
cutaneous sensitivity which occurs in our own bodies only on
exposed mucous surfaces. Such a common chemical sense has
been demonstrated in the frog and in Necturus (Sayle, 1916).
It is difficult to conceive the sensation which must come from the
entire surface of an amphibian's body as the animal moves into
waters of a different acidity.

Whatever may be the nature of the sensations received from
the skin of Amphibia, there is a considerable evidence to indicate
that the tonus of the muscles is maintained by excitations
received from this body cover. Wertheimer (1924) showed that
removing a section of the skin from the thigh of a frog lessens
the tonus of the adjacent muscles. Brief immersions of the
frog's leg in a solution of novocaine had the same effect, while a
return to water brought the tonus back to normal.

Hearing. — One of the most impressive sounds of nature is the
great choruses of frogs in the spring. These arise from the
voices of males and serve to attract females and other males to
the breeding grounds. There is no doubt that some sounds have
considerable significance in the life of frogs. Many male frogs

342

THE BIOLOGY OF THE AMPHIBIA

kept in aquaria will call at the sound of splashing water even
long after their breeding season. But at the sound of the human
voice most Amphibia show no response other than a slowing
down of the respiratory rate in some forms. What significance,
therefore, has sound in the ordinary course of their lives?

Yerkes (1905) showed that sounds had a pronounced indirect
effect on the common frogs, Rana, for if a tactile stimulation
accompanied or soon followed the sound, the response was
greater than it would have been without the sound. The
frog responded to sounds of from 50 to 10,000 vibrations a second.
Yerkes found that the reinforcing influence of sound was greatest
during the breeding season. In one case the influence of the
sound of a wooden gong was much increased by the operation of
cutting away columella and tympanum. This is of interest, for
some frogs, such as Pelobates, lose the columella in the adult and
nevertheless are apparently fully able to hear sounds of their
breeding companions calling in the water. That frogs without a
columella can really hear and not merely feel the sound vibrations
was shown by the fact that Yerkes obtained no further reinforcing
influence when the eighth nerve was cut.

Bruyn and Van Nifterik (1920) have extended these observa-
tions to the European toad. In the case of Rana clamitans,
Yerkes found that if the sound was produced more than one
second before the tactile stimulation no reinforcing influence was
induced. In the toad, Bruyn and Van Nifterik found that there
was a great influence even at an interval of 10 seconds. This
difference of the influence of sound in Rana and Bufo is correlated
with their mode of life. The toad is a roaming terrestrial
animal, and sound is of much greater significance to it than to
the aquatic frog. Once an insect has given away its location by
a sound, the toad is on the qui vive and holds this tuning of
its muscles longer than the frog. In higher vertebrates the
retention of the sound stimulus is of long duration, and hence the
toad may be said to be mentally "higher" than the frog. What
the significance of sounds may mean to tree frogs which locate
their prey at long distances, or to fossorial toads which make little
use of their eyes, has not been demonstrated. Patterson (1920)
found that a whistle caused only slight inhibition of the normal
gastric movements of the bullfrog. It would be interesting to
know if sounds do not influence the stomach contractions of
terrestrial frogs to a greater extent.

THE SENSE ORGANS AND THEIR FUNCTIONS 343

A sense of hearing has been claimed for some salamanders
(Cochran, 1911), but Kuroda (1926) failed to demonstrate it by
laboratory methods. The structure of the auditory apparatus
suggests that salamanders receive vibrations transmitted through
the lower jaw from the substratum when, as larvae, they rest on
the bottoms of ponds. In adult life, vibrations are largely
transmitted through the forelimbs of salamanders. It is prob-
able that sense organs other than the auditory are especially
significant as a warning mechanism in these forms. Unfor-
tunately, the hearing of purely terrestrial salamanders has not
been tested by laboratory methods. Kuroda experimented
with Triturus and Hynobius. He failed to obtain in them the
changes in respiratory movements induced in Rana and Bufo
by a ringing of a bell suspended from the ceiling. Although this
can hardly be considered final proof of deafness, it must be
concluded that a sense of hearing has not been adequately demon-
strated in the Caudata. Vibrations of low frequency in the water
stimulate the lateral-line organs. These can be considered neither
tactile nor auditory organs.

Vision and Sensitivity to Light. — Most Amphibia avoid a
strong light, and many species are nocturnal. The skin of both
frogs and urodeles is sensitive to light rays, even to those which
have been passed through water and freed of all heat waves.
Such light apparently does not produce a painful irritation, for
frogs and salamanders after seeking a retreat in a dark cranny
will frequently turn and face the light. Further, frogs which
had their eyes and cerebral hemispheres removed were found to
turn and jump toward the source of light (Parker, 1903). In
salamanders the skin of the appendages seems more sensitive
to light than that of the body.

The movement of Amphibia toward or away from light has
been assumed to be a tropistic response. Photosensitive
material is apparently present in the skin and is connected by
nerves with the muscles of limbs and body. The tension of
homologous muscles on the two sides of the animal is influenced
in the same mechanical manner as gravity affects them through
the intermediary of the internal ear. The animal will turn
until the tension on the two sets of muscles is the same and will
then continue in as straight a line as the imperfections of its
locomotor apparatus permit. It seems probable that the skin
rather than the eyes serves as the control station receiving the

344

THE BIOLOGY OF THE AMPHIBIA

light waves and directing the tension in the appropriate muscles,
for Cole (1907) showed that a frog possessing only one eye will
orientate itself toward light in the same manner as normal
frogs. The tropistic response is influenced considerably by
external factors. In Necturus the reaction time varies inversely
with the temperature (Cole, 1922). Torelle (1903) found that
Rana pipiens and Rana clamitans are positive to light at ordinary
temperature, while below 10°C. they are negative. This is
doubtless one of the factors inducing frogs to hibernate in the
fall.

There are marked differences in the reactions of different
species to light and these are largely responsible for their dis-
tribution during the day. The larvae of Amby stoma maculatum,
which frequent sunny pools, are positively heliotropic, while the
nocturnal larvae of Eurycea lucifuga and Necturus maculosus
are negative. The marked preference of certain frogs for green
or blue light (Pearse, 1910) might account in part for their
hunting for insects among green grass instead of along exposed
shores of the pond. Frogs, toads, and the newt have a color
vision similar to that of man (Hess, 1910, 1912). They are
able to see food placed in the blue, green, and the red region of
the spectrum with the same acuity as the human eye in a similar
state of adaptation. Further, they have the power of adaptation
of the retina to darkness which resembles but does not equal that
of man.

The phototropism of the Amphibia is overriden by responses
to the field of vision. Regardless of the tropistic action of the
light, frogs and toads are usually attracted by a small object
moving in the field and will attempt to seize and swallow such an
object. But the reaction to these details of the field of vision
are again influenced by other factors. Periods of hunger,
sexual activity, fatigue, and low temperature may greatly alter
the results. Cole (1907) found that at temperatures of 6 to
10°C. Rana clamitans moved toward the smaller of two illumi-
nated areas but that at higher temperatures it went toward the
larger. Further, there are less definable causes which alter the
results. Franz (1913) found that certain frog tadpoles were not
markedly phototropic when swimming in a large tank. When
placed in the confined space of a watch glass they orientated
themselves in the direction of the light. I have found that young
tadpoles of Hyla versicolor in a large vessel swim toward the

THE SENSE ORGANS AND THEIR FUNCTIONS

345

light when the water is disturbed, and this may account for
Franz's results. The phototropic response may be reversed in
Amphibia by feeding. Starved newts are negatively phototropic,
while well-fed ones are either positively phototropic or indifferent
to light (Stier, 1926). Young toads are negatively heliotropic
to strong light (10,0Q0ca.m.) and positively to weak light and to
diffuse daylight and sunlight (Riley, 1913). A similar differen-
tial effect of strong and weak light may account for the well-
known fact that many Amphibia after seeking a dark retreat
turn and face the light. Riley found that if a toad was stimu-
lated by contact with another toad, the former usually turned
and jumped away but frequently followed up the avoiding
reaction by a definite response to light. Thus, mechanical
stimulation may furnish the impulse to locomotion but light is
effective in determining the direction of movement. Young
toads are notably diurnal, while old individuals tend to be
crepuscular or nocturnal in their activities. Laboratory and field
observations have not always been in so close agreement. Lau-
rens (1914) was unable to recognize any phototropic response in
Rana pipiens and Rana sylvatica tadpoles, and yet the former
frequently bask in shallow water. This may, however, be a
temperature response. Cole and Dean (1917) showed that in
Rana clamitans there was a change in phototropism with age.
The young tadpoles were indifferent, the older larvae positively
phototropic. No doubt species differ enormously in the photo-
tropic responses of their larvae.

Amphibia depend, to a large extent, on their vision as the chief
means of obtaining food and avoiding danger. Choruses of
frogs usually cease on the appearance of an intruder, while they
are less affected by the noises he might make. The details of
the visual field may have considerable significance for a frog
which has learned the shape of an object on which his food may
be expected (Biederman, 1927). The size as well as shape of an
object also has significance. Frogs catch insects on the wing.
Salamanders and toads cautiously stalk a fly until within reach
of the tongue. They pause before the snap probably for the
purpose of better fixation (Whitman, 1898). Vision with its
enriched sensory relations gives the Amphibia a great range of
possible responses to their surroundings and this range increases
the opportunities for learning certain tricks in preference to
others.

346 THE BIOLOGY OF THE AMPHIBIA

Rheotropism. — Many salamanders and some frogs live more
or less in streams. When in the water such animals will usually
head upstream and make some effort to stem the current. It
has usually been assumed that stream animals tend to keep their
visual fields the same and that their locomotory efforts against
the current are made for this purpose. But Steinmann (1914)
has reinvestigated the problem in tadpoles and newts and
would attribute the rheotropic response to compensatory reflexes
initiated by the labyrinth. Amphibia, being bilaterally sym-
metrical, tend to move in a straight line. Each deviation stimu-
lates the labyrinth to make compensatory reflex movements of
the muscles to bring it back to the original position. The lateral-
line organs, eye, ear, nose, and other sense organs, exert a supple-
mentary influence on muscle tone. If the homologous sense
organs of either side of the body are equally stimulated, the
muscle tone of the two sides remains the same. Hence, in a
stream, Amphibia would head into the current automatically, if
in contact with the bottom, in order that the stimulation on both
sides of the body might be the same. Steinmann did not work
with typical stream Amphibia and it is possible that these might
respond more to the visual field than the pond forms investigated
in regard to their responses to current.

Thigmotaxis. — Most Amphibia, being nocturnal, are found
during the daylight hours only under logs, stones, and other
debris. Small Appalachian streams in which not a single
salamander may be seen during the day are frequently alive dur-
ing the night with Desmognathus of several species. Toads and
other terrestrial Salientia usually hide away during the daylight
hours in some crevice or burrow. This tendency of Amphibia
to hide is not merely the manifestation of a negative photo-
tropism. Some species appear to be more or less positively
thigmotactic, that is, possess a tendency to move into situations
which will bring a considerable surface of their bodies in contact
with solid objects. Desmognathus fuscus, for example, will take
refuge in glass bottles left lying on the surface of the soil exposed
to the light, usually orientating the body with head toward the
mouth of the bottle (Wilder, 1913). The larvae of the Blind
Salamander, Typhlotriton, has been said to exhibit a greater
positive thigmotaxis than negative phototropism, but observa-
tions by Mrs. Pope and myself have failed to confirm this con-
clusion. The larvae will frequently lie quietly in grooves for

THE SENSE ORGANS AND THEIR FUNCTIONS 347

considerable periods, however, even when exposed to illumina-
tions avoided by the species. There is thus a certain thigmotactic
response in Typhlotriton larvae even though their reaction to
light plays a more important role in sending them to cover.
The same is probably true of most nocturnal Amphibia.

Responses to Internal Stimulation. — The daily movements of
Amphibia are frequently initiated by stimulations from the inter-
nal organs. If the frog or salamander has not fed for some
days there is an increase in the amplitude of the hunger con-
tractions of the stomach. Patterson (1917) has shown that in
the frog this increase is directly proportional to the length of the
fast. The gastric hunger movements of the turtle show a
periodicity, a feature common to higher vertebrates, but both
Necturus and the Bullfrog exhibit continuous contractions of
the stomach (Patterson, 1921) and this may be considered a
more primitive mechanism. The hunger contractions of the
frog stomach are completely inhibited at temperatures below
13 and above 35°C. Since between these limits gastric hunger
movements increase with the temperature, it is apparent that
environmental temperatures have a direct effect on the food-
seeking activity of Amphibia. The bodily changes induced by
anterior pituitary hormone during the breeding season, however,
may prevent these food-seeking reactions of a hungry frog. At
least at the height of the breeding season salamanders and frogs
do not feed.

Szymanski (1918) found there was a daily rhythm in the
activity of Hyla arborea. During July and August there were
two periods daily of activity, with one peak between 12:00 m.
and 1 :00 p. m. and the other between 8 :00 and 9 :00 p. m. The
periods of greatest quiet lay between 5:00 and 6:00 p. m, and 5:00
and 6:00 a. m. It would be interesting to know if the peaks of
activity were controlled by hunger contractions and whether
they could be changed by altering the time of feeding.

Aquatic Amphibia rise frequently to the surface for air. No
doubt the exhaustion of the oxygen supply in the lungs induces
reflexes which lead to the replenishing of the lungs with fresh
air. Amphibia react not only to stimulations impinging upon
them from without, but they also respond to a continuous stream
of impulses coming from their muscles and internal organs.
There are sense organs in the muscles, tendons, and deeper tissues
of the animal which keep it informed as to its posture. Probably

348

THE BIOLOGY OF THE AMPHIBIA

many, if not all, of the impulses from these organs carry no
sensation with them but induce motor effects automatically.
Kinesthetic stimulation may play a part in directing the move-
ments of some Amphibia. Toads which learned their way about
a glass plate continued for several trials to follow this path even
after the glass was removed. The toads may have been directed
by associations involving other sensory mechanisms, however,
as will be indicated in another chapter.

Amphibia, with their moist skins, are in continual danger of
desiccation. Terrestrial forms seek moist situations and absorb
water through their skins. Probably increased osmotic pressure
in the body fluids induced by desiccation releases moisture-
seeking movements. Special sensory receptors concerned with
the sense of thirst have not been described in any vertebrate,
nor have any cutaneous sense organs been reported to be espe-
cially differentiated for detecting differences in humidity.

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Psych., XV, 279-304.

CHAPTER XV

THE NERVOUS SYSTEM

Amphibia respond to external stimulations in a variety of ways.
Living cells from any part of the body have the property of
transmitting excitations, but certain cells, the neurons, are
specialized for this purpose and their fibers are usually grouped
together to form nerves. Cilia on the ectoderm of the embryo
may beat, and heart tissue may pulsate, before any nervous con-
nection has been established with these tissues, but most effector
organs, such as muscles or glands, do not react until they receive
stimulations from the nerves. The latter receive their impulses,
or states of excitation, from the sense organs. The complex series
of nerves which form the nervous system is thus a mechanism
for conducting and correlating impulses received from the sense
organs and transmitting them to organs of response.

A stimulus received at any one point of a nerve cell tends to be
transmitted in all directions throughout its length. In some
invertebrates the nerve cells are possibly joined to form a net,
but in higher types each neuron retains its own identity, a cell
membrane separating the terminal branches of two adjacent cells.
The neurons possess a polarity, certain processes, the dendrites,
conducting the nerve impulses toward the cell body and a usually
longer, less-branching process, the axon, transmitting the impulse
away in the direction of the effector organ. The basis of this
polarity seems to be in the synapse or point of contact between
the axon of one neuron and the dendrites of another. The
state of excitation can be transmitted across the synapse in only
one direction, from the axon of one cell to the dendrites of the
other. Hence, the nerve impulse always travels from the
sensory to the motor neurons. This "law of forward direction,"
first formulated over a hundred years ago, finds its logical
explanation in the theory of the synapse as developed by Sherring-
ton and others. A similar one-way conductivity is found in
the myoneural junction between axon and muscle.

The nerves surrounding the digestive tract of vertebrates
frequently form a plexus, and it has been assumed that this might

353

354

THE BIOLOGY OF THE AMPHIBIA

represent a true nerve net inherited from invertebrate ancestors.
In the frog, however, Cole (1925) has shown that there is a
differentiation within this plexus of axons and dendrites, the
neurons anastomosing only by their dendrites. Further, only
a few nerve cells enter into these fusions, which seem to be a
secondary modification rather than a primitive inheritance.

Reflex Arc. — Neurons are arranged in functional units, the
reflex arcs, each with a neuron receiving the impulse from the

Fun . Lat.

Fig. 124. — Diagrammatic cross-section of the spinal cord of a larval salamander
showing the relation of the sensory to the motor neurons. Corr.N., correlation
neuron; Dor.Rt., dorsal root; Fasc.L.Med., fasciculus longitudinalis medialis;
Fun.Lat., funiculus lateralis; Gr.M., gray matter; My., myotome; S., skin;
Sp.G., spinal ganglion; Tr.B.Sp., tractus bulbo-spinalis; Tr.T.Sp., tractus tecto-
spinal; Tr.Sp.B., tractus spino-bulbaris; T.Sp.Cer., tractus spino-cerebellaris;
Tr.Sp.Tect., tractus spino-tectalis; Vent. H.N. , ventral horn neuron; Vent.Rt.,
ventral root. {After Herrick and Coghill.)

sense organ, another neuron transmitting it to an effector organ,
and, generally, a third intercalated between the two (Fig. 124).
Reflex arcs are usually complicated by the addition of several
cells of this third category; twigs from their axons, called "col-
laterals," making possible the transmission of impulses to several
adjustors or effectors. The passage of an impulse through a
reflex arc requires more time than is consumed by the impulse
traveling the same length of nerve and stimulating the same
end organ alone. Hence, the synapse and the myoneural
junction apparently present some functional modification in the

THE NERVOUS SYSTEM

355

passage of an impulse. The delay increases with the number of
synapses involved in the arc. Nervous impulses are transmitted
at different rates in different fibers, the rates being much greater
in medullated than in non-medullated nerves, and greater in
fibers of large than in those of small diameter. Possibly some of
the delay in the passage of an impulse through a reflex arc is due
to the small fibers of the central nervous system. Drugs may be
employed to increase or lower the conductivity of impulses,
presumably at the synapses, and no doubt the physiological
condition of the animal, as, for example, the amount of oxygen
in the blood, has a marked effect on conduction over the synapses.
In brief, the character of a reflex is dependent not only on the
structure of the arc but also on the functional conditions which
exist at any one time throughout the system.

Repeated use of particular paths of conduction increases their
conductivity for succeeding impulses. This is apparently due to a
change in the synapse which makes it less resistant to excitations.
The synaptic change apparently forms the basis of learning,
although it is possible that other phenomena, such as combined
activity of great numbers of neurons or, during an early stage
of development, the growth of the axons or dendrites, may play
some role. The process of synaptic change is reversible — a pos-
sible explanation of the loss of learned responses or of forgetting.

The repetition of a stimulus may produce other effects. If a
single stimulation is not adequate to produce a response, the
repetition of this stimulus at frequent intervals may have the
desired effect, apparently because the resistance at the synapse is
lowered by the repetition. Continued stimulation, however,
will eventually lead to failure of response, apparently as a result
of the fatigue products acting at the synapse. Frequently the
result of a stimulation is the inhibition of an activity. This has
been interpreted as due to increase of resistance at the synapse,
the refractory period of the synapse having been prolonged by
too great frequency of the impulses arriving there. According
to this explanation, each successive excitation of the nerve
would fall within the refractory phase, and no response would
result.

The axons of many of the neurons are covered by a white
fatty substance, the myelin sheath, which apparently serves to
insulate them, preventing impulses in adjacent axons from
influencing one another. Some fibers are covered merely by a

356

THE BIOLOGY OF THE AMPHIBIA

nucleated membrane as in many of the axons of both the central
and sympathetic nervous systems. In many parts of the central
nervous system several nerve cells of one functional type occur
together, forming a center or nucleus. A grouping of nerve cell
bodies outside of the central nervous system is called a " gan-
glion." The larger groupings of nerves into systems may be
conveniently considered under the divisions: brain, spinal cord,
and autonomic system.

Brain. — Amphibia inherited their brains as well as the remain-
der of their organization from piscine ancestors. The primitive
crossopterygian fishes left in their fossilized skulls little evidence
of the type of brain they possessed, but the dipnoans, which
sprang from a closely related stock, possess a brain which is
essentially like that of the Amphibia both in its method of
development and in the arrangement of nuclei and commissures.
We may assume that the crossopterygian ancestors of Amphibia
had a similar brain. The most distinctive feature of this brain
was the evagination of the hemispheres, the latter constructed
on the same plan as the hemispheres of higher vertebrates and
contrasted with the everted forebrain of teleosts, with its mem-
branous non-nervous roof. Herrick (1921, 1924) has suggested
that this type of forebrain was originally an adaptation to life
in poorly oxygenated water. The nervous tissues secure their
supply of oxygen not only from the blood but also from the
cerebrospinal fluid, and the latter would be excluded from
the interior of thickenings of nervous tissue such as is found in the
forebrain of teleosts. Solid masses of nuclei such as are found
surrounding the ventricles of some fish and birds are well adapted
for the performance of complex types of instinctive habits, but
thin-walled, widely evaginated cerebral hemispheres, capable of
indefinite expansion without a great thickening of the wall, were
more suitable as a foundation for the elaboration of the mamma-
lian brain with its capacity for rapid learning.

In spite of the great potentiality for future development found
in the forebrain of Amphibia, no great progress in this direction
was made by modern Amphibia. This is because they have still
retained for the most part the primitive arrangement of the nerve-
cell bodies around the ventricles, while the nerve fibers lie external
to them as an unbroken aggregation of white matter. The
road to advancement lay through the development of a more
diffuse distribution of the cell bodies and their fibers, also in the

THE NERVOUS SYSTEM

357

aggregation of special clusters of cells to discharge in fiber paths
having specific functions.

The brain arises during development by a differentiation of the
anterior part of the neural plate, the edges of which roll over
during gastrulation to form a tube. Very early three enlarge-
ments common to the brains of all vertebrates develop. These
are the forebrain, midbrain and hindbrain. The forebrain again
becomes differentiated into a telencephalon and a thalamen-
cephalon, while the hindbrain develops a cerebellum poorly
marked off from the remainder of the hindbrain, the medulla
oblongata. Thickenings or other differentiations appear in all
five regions. The original cavity of the tube remains to form the
ventricles of the brain.

A B C

Fig. 125. — Diagrammatic cross-section of the forebrains of (A) salamander,
(B) frog, and ((7) caecilian, to show the principal nuclei. B., nucleus basalis;
B.S., nucleus basimedialis superior; Co., cortex olfactoria; D., area dorsalis
pallii; L., area lateralis pallii; M., area medialis pallii. (After Kuhlenbeck.)

Forebrain. — The forebrain of Salientia is shorter and more
compressed than that of most urodeles. Nevertheless, the
evagination of the hemispheres is carried farther, since the
unpaired ventricle at the posterior end is smaller in frogs than in
urodeles. Two enlargements at the anterior end of the hemi-
spheres are the olfactory lobes from which the olfactory nerves
arise. They are ventral in Hynobius as in frogs, but in the latter
they are fused in the midline. The ventral position of the lobes
is probably primitive, although in most urodeles they have a
more lateral position, markedly so in the newt and in Siren.
In the specialized Eurycea the lobes are also ventral (Rothig

358

THE BIOLOGY OF THE AMPHIBIA

1912). In the Gymnophiona they are very large and ring
shaped but separate, as in the salamanders (Kuhlenbeck, 1922).

Each cerebral hemisphere may be divided into a dorsal pallium
and a ventral subpallium. In the Salientia a groove on the sur-
face separates one region from the other and limiting sulci occur
on the inner surface of the ventricles in most Amphibia. A fur-
ther division into an internal hippocampus and external pyriform
primordium of the pallium, and an internal septum and an external
striatum of the subpallium, is indicated by the distribution of
the nerve bundles and cell groups within each hemishhere
(Fig. 125).

In urodeles the septum or ventral median nucleus is not large,
although in various species, such as Cryptobranchus and Siren,
it is sufficiently developed to form an eminentia septalis which
projects into the ventricle (Rothig, 1912). In the Salientia there
is a hypertrophy of the septal regions which are proportionately
further developed than in any vertebrate (Kiesewalter, 1928) .

Fibers from the olfactory bulbs extend to nearly all parts of
the cerebral hemisphere. The anterior olfactory nucleus and
parts of the pyriform area are largely made up of incoming fibers.
The septum and striatum are chiefly synaptic stations where
olfactory fibers join with ascending and descending fibers from the
thalamus and midbrain. The striatum of urodeles is relatively
undifferentiated, the cell bodies maintaining for the most part
their primitive periventricular position. The elaboration of the
striatum is correlated in part with the development of Jacobson's
organ (Herrick, 1921a) and in part with the increase in exterocep-
tive tracts. Thus, Necturus and Proteus, being larval types
without a Jacobson's organ, have a very poorly developed striatum,
while the Salientia and Gymnophiona, with their large Jacobson's
organs, approach the reptiles in the enlargement of this region.
Jacobson's organ is a mechanism for testing the contents of the
mouth and it arose as an important aid to terrestrialism. Corre-
lated with the development of this organ, there appeared an
accessory olfactory lobe on each side, a well-defined ventral
lateral nerve tract within the hemisphere, and an amygdaloid
nucleus in the striatum. Plethodontids, although advanced
types, have small Jacobson's organs and relatively undifferen-
tiated forebrains (Herrick, 1921). In the Salientia there is an
outward migration of striatal cells, well marked even in the
tadpoles (Soderberg, 1922). In the Gymnophiona a true cortex

THE NERVOUS SYSTEM

359

or correlation center of laminated cells is formed in the outer
portion of the striatum separate from the periventricular series
(Kuhlenbeck, 1922). In higher vertebrates the striatum becomes
one of the chief reflex centers governing motor reactions by reason
of its tract connections with lower and higher centers (projection
tracts), but in the Amphibia it is still dominated by the olfactory
components (Herrick, 1927).

The hippocampus and pyriform areas show a wandering of cells
toward the periphery, which is carried farther in Salientia than

Fig. 126. — Plan of the chief fibre tracts in the brain of the frog, a.c, anterior
commissure; amy., amygdala; a.t., acoustic tubercle; b.c, brachium conjunctivum;
c.b., cerebellum; ch.p., chorioid plexus; dor., dorsal nucleus of the thalamus; d.s.c,
dorsal spino-cerebellar tract; g.c, geniculate or postoptic commissure; hb.,
habenula; hip., hippocampus; hp., habenulo-peduncular tract; i.e., inferior
colliculus; l.g., lateral geniculate body; l.L, lateral lemniscus; m.o.t., medial
olfactory tract; m.p., mamillary peduncle; n.p.c, nucleus of the posterior com-
missure; o.b. , olfactory bulb; o.h., olfacto-habenular tract; ol.n., olfactory nerve;
ol.p., olfacto-peduncular tract or medial forebrain bundle; ol.s., olfacto-septal
fibres; ora., oculomotor nerve; ost., striatal nucleus; o.t., optic tract; p.c,
posterior commissure; pit., pituitary body (hypophysis); r.n., red nucleus; s.h.,
septo-hippocampal fibres; s.t., spino-tectal tract; s.t.p., lateral forebrain bundle;
t.c, tuber cinereum of hypothalamus; th.s., septo-thalamic tract or medial
forebrain bundle; t.s., tecto-bulbar and tecto-spinal tract; tub., olfactory tubercle;
v.m., vestibulo-mesencephalic tract; v.s., vestibulo-spinal tract. (After Papez.)

in urodeles (Kiesewalter, 1928; Kuhlenbeck, 1929). This
corticogenesis does not reach in the adult frog the extreme found
in the striatum of tadpoles or of Gymnophiona. Such wandering
of cells leads in reptiles and in mammals to the development of
cell laminae in the pallium well separated from the periventricular
cells (Kiesewalter, 1928). They become correlation centers,
while the latter remain pathways for relatively simple reflexes.
With the development of a cortex there is an increase in the
number of non-olfactory fibers which make their way from the
thalamus into the forebrain (Fig. 126). Some of these ascending
fibers are already present in the forebrain of Amphibia. Binde-

360

THE BIOLOGY OF THE AMPHIBIA

wald (1914) and Herrick (1927) consider the striatum to represent
an olfactotactile and olfactovisceral center. This integration of
olfactory with other senses is still largely of a reflex character.
The development of a cortex adds more sensory data, and more
possible routes for impulses to travel. It introduces hesitancy
into behavior and opportunity for training to influence the final
efferent path selected. Although fishes and Amphibia have some
associational tissue and are able to learn, the Gymnophiona have
developed a distinct basal cortex. The pallial cortex first appears
in reptiles. Further, in Amphibia there are no tracts leading
directly from the forebrain to any centers below the level of the
midbrain as in higher forms (Von Monakow, 1910). Thus, while
in mammals injury to the pallial cortex greatly affects the reac-
tions of the animal, frogs deprived of their entire forebrain swim,
feed, and breed very much as do normal frogs (Schrader, 1887).
Decerebrate frogs lack a certain spontaneity of reaction (Loeser,
1905). Variety of response is erased, for distracting or confusing
sensory impulses are ruled out by the operation. Since the
result is the same even when olfactory impulses are not involved,
it is clear that the forebrain functions in correlating various sen-
sory data, if only into reflex patterns. Electric stimulation of the
forebrain of Amphibia leads to no motor response (Bickel, 1898;
Chauchard, 1927), hence the contribution of nerve impulses
from this region is primarily sensory.

Thalamus. — Immediately caudal to the unpaired forebrain
is the thalamus. From this region of the brain the optic vesicles
arise as evaginations. The retinas agree with the cerebral
hemispheres in being outpockets of the brain. The optic nerve
(Fig. 127) consists of tertiary fibers, two synapses having occurred
in the sense organ itself, namely, within the eyeball. The optic
nerve enters the anterior, ventral border of the thalamus, all the
fibers crossing to the side opposite the retina of their origin before
curving up around the thalamus to penetrate the midbrain behind.

Two other afferent nerves enter the thalamus on each side.
The nervus terminalis enters the forebrain at the ventral border
of the olfactory lobe in Necturus (McKibben, 1911), continues
back to the superficial border of the hemispheres, and penetrates
the thalamus ventrolateral^ to extend as far as the posterior
tubercle (Herrick, 1927). The exact function of this nerve is
unknown, but it probably receives stimuli from sense organs of
the snout. The second afferent nerve is the parietal, which

THE NERVOUS SYSTEM

361

extends from the pineal organ to the region of the posterior
tubercle. The pineal organ arises as a dorsal evagination of
the thalamus and seems to have important endocrine functions.
Whether or not it is really sensory at any stage of development is a
disputed point. Since a pineal foramen is present in the skulls of
some fossil Amphibia, it was probably originally a sensory organ,

/ nasal sac /,

: .'choariQ; /

Fig. 127. — Ventral aspect of the brain of Necturus showing relation of cranial
nerves to nasal sac, eye, and ear. {After McKibben.)

a third eye, as in some modern reptiles. The pineal organ is
best developed among many modern Amphibia in the larvae.

The peripheral connections of the midbrain may be considered
with those of the thalamus. The mesencephalic root of the trigem-
inus nerve enters the posterior part of the midbrain and makes
important connections with the optic fibers. The two eye-muscle
nerves, oculomotor and trochlear, enter the midbrain as in all
vertebrates. The first supplies the superior and inferior rectus
muscles and the inferior oblique. The latter supplies the superior

362 THE BIOLOGY OF THE AMPHIBIA

oblique alone. The lateral rectus muscles of the eye are inner-
vated through the abducens, which enters ventrally in the anterior
part of the medulla. The retractor bulbi, well developed in the
Salientia, is innervated in part through the abducens and in
part through fibers (of sympathetic origin) coming from the
ciliary ganglion (Gaupp, 1899).

In passing through the thalamus on the way to the midbrain
roof, the optic nerves give off many collaterals which make synap-
tic connections with other sensory systems. In the epithalamus
or habenula, optic fibers are joined in synapse with olfactory
fibers. The hypothalamus, on the other hand, is a center of
visceral correlation where taste and impulses from the digestive
tract are integrated with smell (Herrick, 1917; Rothig, 1926).
The thalamus of Necturus has a diffuse field of synaptic con-
nections, while in Ambystoma there is a tendency for localization
of groups of synapses. Nevertheless, the general arrangement of
nuclei in the thalamus is essentially the same not only in all
Amphibia but in all Anamnia (Kuhlenbeck, 1929a).

Midbrain Roof. — The roof of the midbrain receives the bulk
of the optic fibers. In most Amphibia it forms a prominent
swelling on the dorsal surface of the brain. In Salientia with
well-developed eyes, it is a bilobed structure, the two parts
forming the optic lobes. In urodeles the eyes are usually smaller
and the midbrain roof is less swollen and without a division into
well-marked lobes. As in fish, the optic lobes are the center of
vision. In higher vertebrates most optic fibers end in the
thalamus, where they form a synaptic junction with fibers of the
optic radiation to the visual cortex of the forebrain. Amphibians
are of interest, for they show the first stage in this transference of
the optic center ; many of the optic fibers in passing through the
thalamus send off collaterals there. Herrick (1925) describes
three important aggregations of synaptic connections in the
thalamus related to the optic system and these are especially
well defined in Salientia. Further, in some forms, especially in
adult frogs, there is an extension of the optic fibers into the
cerebral hemispheres. They form the thalamofrontal tract which
in mammals is destined to become the optic radiation. The
enlarged eyes of the frog may be responsible in part for the
bilobed roof of the midbrain and the radiation of optic tracts
into the forebrain. In the small-eyed Pipa (Fig. 128A) the
optic lobes are large but confluent, as in most urodeles (Gronberg,

THE NERVOUS SYSTEM

363

1894). In mammals somesthetic tracts penetrate the region to
form an inferior colliculus on each side. As a result, the mid-
brain roof becomes quadripartite to form the corpora quadri-
gemina. In Amphibia a root from the trigeminus and the
sensory lemniscus fibers bring in a variety of sensory data, includ-
ing impulses from tactile organs, lateral-line components, and
proprioceptive centers for integration with the optic impulses. A
rudiment of the inferior colliculus is present in all Amphibia but is
more pronounced in Salientia than urodeles. In Pipa it is most
emphasized, an interesting parallelism to the condition in
mammals. The cells which effect these synapses in the midbrain
roof tend to align themselves in layers of functionally different
nerves. In Necturus these are large neurons covering more or
less of the entire roof, in Ambystoma they are small and show
some lamination, while in Salientia the stratification is well
established.

The base of the midbrain or cerebral peduncles transmits the
motor impulses to lower levels. These peduncles include the
nucleus of the motor tegmentum and embrace the final common
motor paths for which the sensory impulses of forebrain, thala-
mus, and midbrain compete.

An experimental investigation of the midbrain and thalamus
has confirmed and further extended the conclusion reached as
to the function of these parts of the brain. Chauchard (1927)
showed that an electric stimulation of the anterior part of the
optic lobes induced a movement of the hind limbs, a similar
stimulation of the posterior part effected a forelimb movement,
while the middle-region stimulation brought movements in the
eye muscles. Baglioni (1911) had previously shown that the
grasping reflex could be produced in the male frog by electrical
stimulation of the optic lobes. In view of the importance of body
size of the female in sex recognition in frogs, it is interesting that
Schrader (1887) should have found that removal of the optic
lobes caused a loss in the sense of touch. The ablation of these
lobes also induced a permanent darkening of the coloration.
Color change is known to be affected in many Amphibia by both
sight and touch; and in view of these experiments it would seem
that the correlation was effected in the midbrain. Stimulation
of the midbrain had the further effect of profoundly altering the
respiratory rate (Martin, 1878). In higher vertebrates the
thoracic muscles of respiration find their centers of control in this

364

THE BIOLOGY OF THE AMPHIBIA

region, and possibly the midbrain controls pharyngeal respiration
in Amphibia (Babak 1913).

Cerebellum. — The two posterior parts of the brain, cerebellum
and medulla, are intimately related, the former being a dorsal
growth from the latter. The cerebellum consists of a medial pair
of corpora cerebelli and a more lateral pair of auricular lobes
which form a direct continuation of the acousticolateral area
of the medulla from which they arise during their development
(Herrick, 1914). The corpora cerebelli do not form a middorsal
connection in Necturus and Amphiuma as in most Amphibia.
The cerebellum of fish is more highly developed than in any
Amphibia and there is a great elaboration of the auricular lobes
in correlation with the extensive lateral-line system. The reduc-
tion of the corpora cerebelli in Amphibia is correlated with their
simple locomotory movements. The cerebellum is generally
considered to be the station controlling postural activity, inte-
grating impulses from the organs of equilibrium with those of
muscle tone, but injuries to the medulla of the frog evoke
disturbances of locomotion and posture usually attributed to
defects in the cerebellum (Loeser, 1905). It would seem that
some of the components usually found in the cerebellum occur
in the anterior portion of the medulla, particularly in the
acousticolateral area.

The chief peripheral connection of the cerebellum is with the
auditory nerve. The mesencephalic root of the trigeminus passes
through the cerebellum but has no terminals there in urodeles
as it has in Salientia. The cerebellum is proportionately larger
in the larval Ambystoma than in the adult. At metamorphosis
there is a reduction of the auricular lobe in aquatic Amphibia due
to the disappearance of the lateral-line system and only vestibular
components are left in the auricular lobes (Larsell, 1925). In
Salientia, at least, there is a loss of the lateral-line connection
from cerebellum to hypothalamus. Tadpoles would seem to
have an important lateral-line and possible gustatory control
over their movements, while in the adult frog a vestibular-optic
control replaces it. As in the case of forebrain and thalamus, this
control of the cerebellum is by the integration of sensory rather
than motor components. The character of the Purkinje cells
of the cerebellum together with their lamination is adapted to the
summation, reinforcement and diffusion of excitations. The
histological structure of the cerebellum of Salientia is more com-

THE NERVOUS SYSTEM

365

plex than that of urodeles. The first indication of a true cere-
bellar nucleus appears, as well as the beginnings of the dentate
nucleus of higher forms with its important descending tracts
to the peduncles of the midbrain. Further, the Purkinje cells in
Salientia have a far more definitive structure than in urodeles,
and there is a true lamination of the cells and fibers.

Medulla. — The medulla, the most posterior part of the brain,
has the appearance of a slightly widened and flattened portion of
the spinal cord. Its dorsal surface is, however, largely mem-
branous and a cluster of blood vessels forms as the choroid plexus,
a vascular diverticulum of this membrane, extending into its
ventricle. Like the spinal cord, the medulla is divided into a
basal medial motor region and a dorsal sensory area which,
because of the membranous roof, is largely lateral. The fifth
to tenth cranial nerves enter the medulla and bifurcate to send
ascending and descending fibers of specific functions the length
of the medulla (Kuhlenbeck, 1927; Kappers and Fortuyn,
1921). The dorsal zone is the acousticolateral area. This
forms the rhomboidal lip which merges directly into the auricular
lobe of the cerebellum. The medial longitudinal zone is formed
by the visceral sensory fibers of the seventh, ninth, and tenth
cranial nerves. The ventral sensory zone of the medulla is
formed by cutaneous sensory fibers of the fifth and tenth nerves.

The Amphibia are noteworthy in showing the first rudiment of
the cochlea of higher vertebrates. In correlation with division of
function in the inner ear, there are two centers for the eighth
nerve in the medulla of frogs, the vestibular nucleus being the
more ventral. With the appearance of a separate dorsal nucleus
in Salientia there is also found an acoustic center homologous to
the superior olive of mammals which is concerned in the trans-
mission of acoustic impulses from the eighth cranial nerve to the
midbrain. It may also have a more direct connection with the
motor portion of the cord.

Between the dorsal and ventral portions of the medulla lies
the reticular formation or region of synaptic junction between
sensory and motor fibers. In the anterior part of this region in
urodeles occur the giant cells of Mauthner which send their axons
throughout the length of the spinal cord to the tail musculature
and function in the regulation of swimming movements (Detwiler,
1927a). Vestibular and lateral-line fibers make synaptic con-
nections with these cells.

366

THE BIOLOGY OF THE AMPHIBIA

In the ventral motor portion of the medulla the nuclei of the
third to twelfth cranial nerves are arranged in their numerical
order. In primitive Amphibia more of the medulla was contained
within the skull than in modern Amphibia, for all 12 cranial
nerves made exit from the skull as in mammals. In recent
Amphibia the twelfth nerve and the eleventh, when present, lie
beyond the skull and form spinal nerves. The frogs show a
greater separation of the motor nuclei from one another than do
the urodeles. This is particularly true of the nuclei of the
seventh, ninth, and tenth nerves. Also, the sensory nuclei of
the fifth and seventh nerves show anastomosis in urodeles, not
present in the Salientia.

The reaction of frogs after removal of various parts of the
medulla confirms the conclusions reached from an examination of
the structure of this part of the brain. Few motor responses
are controlled by any one level alone. The croaking reflex
which is influenced by the optic lobes persists if the medulla
is retained (Steiner, 1885; Schrader, 1887). The swallowing
reflex is initiated primarily by impulses from the trigeminus. It is
produced by efferent fibers in the facialis. The movements of the
tongue depend on the function of the hypoglossus nerve, and they
persist after the destruction of the swallowing reflex mechanism
(Schrader, 1887). Locomotion is more dependent on caudal
than on cephalic levels of the medulla according to Schrader
(1887), but some motor coordination of the limbs can be main-
tained by the spinal cord alone (Goltz, 1869). As stated above,
some of the locomotor postural functions controlled by the
cerebellum of higher forms are assumed by the medulla of
Amphibia. In urodeles Mauthner's cells seem to have an impor-
tant role in swimming movements. Control over respiration is in
part effected by the vagus fibers with their center in the medulla
(Baglioni, 1900). Pharyngeal, nasal, and other muscles are
actively concerned in buccal respiration, however. Hence, all
levels of the medulla are probably concerned in the respiratory
cycle, and impulses from the midbrain may modify the action.
The vagus, with its center in the medulla, has further both a
digestive and a vasomotor control (Bottazzi, 1899, 190-1), the
primitive character of the vagus being that of a digestive nerve
and the other functions being only gradually acquired in the
course of vertebrate evolution. Muchin (1895), by electric
stimulation of the medulla, was able to induce movements of the

THE NERVOUS SYSTEM

367

eye, maxillary muscles, tongue, or head according to whether he
stimulated the region of the abducens, facialis, hypoglossus, or
vagus centers. It is seen from this discussion that the midbrain
and medulla hold centers involving most of the important
responses of the animal to both the internal and external environ-
ment. This is true of most cold-blooded forms, where the mid-
brain particularly performs functions largely relegated to
anterior levels of the brain in higher vertebrates.

Phylogeny of the Brain. — The progressive modification of the
brain as a whole does not follow closely the phylogenetic scheme.
The simplicity of the brain of Necturus seems in all probability
to be a retained larval character. But Siren, which is also chiefly
larval in organization, exhibits a well-marked development of the
septal region of the forebrain (Rothig, 1912). The Salientia,
which stand nearer the branchiosaur ancestors in most of their
skeletal organization than do the urodeles, have a greater develop-
ment of the corpus striatum, a truly reptilian character. Soder-
berg (1922) and Kuhlenbeck (1927) considered the brain of the
Salientia more primitive than that of the urodeles. The chief
evidence Soderberg brought forward for this conclusion was the
supposed retrogressive change at the time of metamorphosis in
tadpoles. It might also be added that as the labyrinthodonts
stood nearer the reptiles in their skeleton than do modern
Amphibia, they probably did likewise in their brains. The
urodele brain is more schematic than that of the frogs and hence
has been more secondarily modified.

The Gymnophiona, which may have evolved from lepospondyls
instead of branchiosaurs, have a brain modified by a regression
of the optic centers and an elaboration of the olfactory ones.
As Kuhlenbeck (1922) showed in Hypogeophis, the forebrain and
especially its basal parts are greatly elaborated (Fig. 128C),
while the thalamus, midbrain, and cerebellum are insignificant.
The Gymnophiona approach the reptiles in the great develop-
ment of the striatum and in the flexure of the medulla. Since
the Gymnophiona lead such a specialized life, it is difficult to
decide whether or not these features are primitive amphibian
characters. Both Kuhlenbeck (1922) and Schmid (1929) find
various similarities between the brains of Gymnophiona and
urodeles not shared by the Salientia.

A retrogressive change in the brains of Amphibia might have
been caused by a degeneration of sense organs. Destroying the

368

THE BIOLOGY OF THE AMPHIBIA

eye of the growing tadpole brings about marked reduction in the
midbrain (Durken 1912). The converse experiment of building
up the brain by increasing a sensory area has been performed
on Ambystoma. Burr (1922) transplanted the large olfactory
placode of Ambystoma tigrinum on the small A. maculatum and
obtained an increase in the number of cells of the cerebral hemi-
sphere of the host. This increase extended to the secondary and
tertiary nuclear centers. Thus, axons growing into embryonic

Fig. 128. — Amphibian brains, dorsal view. A. Adult Pipa pipa. {After
Griinberg.) B. Larva of Hynobius nebulosus. (After Sumi.) C. Adult Hypo-
geophis rostratus. (After Kuhlenbeck.) C, cerebellum; E.M.R., eminentia
medialis rhombencephali ; Ep., epiphysis; F., fossa rhomboidea; H., lobus
hemisphaericus ; M., mesencephalon; N.I.-N.XI., cranial nerves I-XI; O.,
nervus olfactorius; Par., paraphysis; S.Lg.C, sulcus longitudinalis centralis;
S.R.A., sulcus rhinalis anterior; S.T.D., sulcus transversus diencephalo-
mesencephalicus ; T., thalamus.

brain tissue are potent factors in the further elaboration of the
brain.

Such experiments are very suggestive of the way the brain
was built up during phylogeny. An increased growth in one
center might have a corresponding effect on another. An
equally important change in phylogeny was the grouping of
nerves of related functions in discrete areas. Such a progressive
change has only well begun in the Amphibia. In the higher
vertebrates there is an attraction of most of the somatic connec-
tions to the striatum and later their projection to separate centers
on the pallium. Such a brain is far better adapted both for

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369

judging and for learning than the brain of Amphibia. The fore-
brain and thalamus of Amphibia are still only accessories and not
full-fledged essentials of all reactions, as in mammals. The
brain evolution of higher vertebrates, however, is made along
lines first clearly indicated by the amphibians. The further
integration of sensory components and their intimate connections
with motor activity gradually brought about an increasingly
specific reaction to significant factors of the environment. With
the specialization of hands, feet, and other structures as complex
organs of response, there arose within each dominant system of
final common paths many subsidiary systems, each requiring
its own central ad just or, above which developed the higher cen-
ters of correlation. These correlation centers arose at the chief
cross-roads of impulse traffic, namely, reticular formation, cere-
bellum, midbrain, thalamus, and corpus striatum (Herrick,
1929).

Spinal Cord and Nerves. — The spinal cord arises in the same
way as the brain by the folding over and fusion of the margins of
the neural plate. Like most of the brain it may be divided into a
dorsal afferent and ventral efferent series of fiber tracts and related
centers. In cross-section the spinal cord of Amphibia resembles
that of other vertebrates in having a typical butterfly-like arrange-
ment of gray matter surrounding the central canal or lumen
resulting from the inturned neural plate. The most dorsal por-
tion of the wings is formed by nuclei where somatic afferent fibers
terminate; more ventral are the visceral afferent centers. The
lower portion of the wings is formed by the visceral efferent cell
bodies above and the somatic efferent ones below. The axons
extending from these centers form the surrounding white matter
of the cord. Some fibers are confined to one segment but the
great majority extend forward or backward along the cord.
Further, axons from the medulla may extend for varying dis-
tances into the cord. In the frog, fibers extend from the ninth
and tenth cranial nerves to the second and third spinal segments,
from the eighth nerve as far as the sixth segment, from the fifth
nerve to the lumbar enlargements, while fibers from Mauthner's
cells extend the length of the cord (Kuhlenbeck, 1929).

The cord is supplied with a series of spinal nerves which may
be as few as 10 or 11 pairs in frogs. Each spinal nerve arises
from the cord by two roots : a dorsal one containing sensory fibers
running to the cord and a ventral one with motor fibers leading

370

THE BIOLOGY OF THE AMPHIBIA

away from it. The sensory fibers of the nerve have their cell
bodies in the ganglion of the dorsal root, while those of the motor
components are contained within the spinal cord. The former
position is very probably secondary, since the spinal ganglia
arise from a neural crest or laterally extended margin of the neural
plate. It is interesting that some urodele larvae during early
development contain sensory cell bodies still within the spinal
cord. These are the Rohon-Beard cells which receive sensory
impulses from the muscles with some of their dendrites, from the
skin with others, and send axons conducting these impulses
forward. Such an arrangement is probably a primitive verte-
brate condition.

The dorsal and ventral roots unite close to the vertebral column
to form a mixed nerve, which divides again into a dorsal branch
supplying the skin and muscles of the upper surface of the body
and a ventral branch innervating the ventral and limb muscles.
Several of these ventral rami unite in the brachial and pelvic
regions to form plexuses. Such plexuses, although considered
homologous in frog and salamander, may be formed of different
spinal nerves. The growing limb bud has been shown by
experiment (Detwiler, 1927) to attract the spinal nerves. Fore-
limb buds transplanted over six segments posterior to their
original position induce new spinal nerves to innervate them.

The visceral fibers of the nerve roots extend into the ventral
ramus of the mixed nerve for a short distance and then leave as a
ramus communicans to end in the sympathetic ganglia. In this
way visceral efferent fibers never extend all the way from spinal
cord to smooth muscle or gland without a synapse in the periphery.

The chief function of the spinal cord is that of a motor effector.
The hind and midbrain have an important control over loco-
motion, but the limbs alone, if properly stimulated, can perform
normal locomotor movements provided their centers in the spinal
cord are left intact (Loeser, 1905). Van Rynberk (1909) placed
the center controlling forelimb movements in the second spinal
segment. A severe injury to the spinal column in mammals will
usually prevent all movement in the hind limbs, but the spinal
column of salamanders may be sectioned between fore- and hind
limb without preventing the synchronous movements of the limbs
in walking (Snyder, 1904; Ten Cate, 1928). In this case the
afferent stimulus for releasing walking movements of the hind
limbs would seem to be the slight tactile stimulation to the soles

THE NERVOUS SYSTEM

371

of the hind feet on being dragged forward by the forelimbs.
Coordinated movements of the limbs cease after sectioning of the
dorsal root (Hering, 1897). Nicholas (1928) found that in
Ambystoma larvae, after removing a large section of the spinal
cord, there was still coordination between fore- and hind limbs.
This he attributed to the pull of the body muscles transferring
stimulations between the two segments. The relations of these
stimulations to normal locomotion will be considered in the
discussion of habits.

The coordination of movement between the members of any
one pair of limbs is controlled by nervous connections within the
spinal cord. In the case of the forelimbs of Ambystoma macula-
turn, this coordination is accomplished by the fifth spinal nerve
and its spinal connections. Grafted limbs which receive only a
very small branch of this nerve carry out well-defined coordinated
movements in both forearm and hand (Detwiler and Carpenter,
1929) . Further, severing the sixth and seventh spinal nerves does
not prevent coordinated function in the graft. There can be no
extensor or flexor nerve in this case, but a very extensive branch-
ing of the fifth nerve within the muscles must occur to bring
about the various limb movements. Limbs grafted to the ear
region of Ambystoma move synchronously or alternately with
the swallowing or gill movements (Detwiler, 1930), because their
motor nerves are derived from the nerves of this region and hence
have the same central connections.

Autonomic System. — The name autonomic system is given to
that part of the peripheral nervous system which innervates
smooth muscles and glands. It is autonomic in the sense of hav-
ing its own series of ganglia isolated from the central nervous sys-
tem but connected with it by the rami communicantes (Fig. 129).
The cell bodies of most somatic sensory neurons also lie outside
the central nervous system in the dorsal root of the spinal nerves
or near the base of cranial nerves. These form sensory and not
motor ganglia, as in the present case, however. The autonomic
system consists of a cranio-sacral or parasympathetic out-
flow and a thoracico-lumbar or sympathetic outflow. Although
afferent visceral neurons accompany the efferent neurons, they
have their ganglia in the dorsal roots and extend all the way
from the sense organs to the central nervous system and hence
conform to the ordinary type of somatic afferent fibers. The
parasympathetic outflow consists essentially of visceral fibers

372

THE BIOLOGY OF THE AMPHIBIA

Cerv. Sym.

\Abd. Sym.

">Caud. Sym.

Fig. 129. — The autonomic nervous system of Necturus. Abd. Sym., abdomi-
nal sympathetic; A.C., coeliac artery; Ac, aorta caudalis; A.M., mesenteric
artery; Ao., aorta; A.R., renal artery; A.S., subclavian artery; Caud. Sym.,
caudal sympathetic; Cerv. Sym., cervical portion of sympathetic system; C.G.,
first cervical ganglion; CI., cloaca; Gl., ramus glossopharyngeus of the vagus;
G.S.A., anterior subclavian ganglion; G.S.L., lateral subclavian ganglion; G.S.P;
posterior subclavian ganglion; G.V., vagus ganglion; Hm., hyomandibular branch
of the facial nerve; In., ramus intestinalis of N. vagi; M.D., Mtillerian duct;
N.Sp.A,. anterior splanchnic nerve; N.Sp.P., posterior splanchnic nerve; P.K., pel-
vic kidney; R.A., anterior ramus of the vagus; R.Ao., radix aortae (root of aorta) ;

THE NERVOUS SYSTEM 373

of the vagus system, innervating respiratory, digestive, and cir-
culatory structures. Associated with these are fibers from the
third, seventh, and ninth cranial nerves. Kuntz (1911) has
traced the peripheral wandering of parasympathetic ganglion
cells from the hind brain of the frog along the paths of the vagi
and has established their morphological identity with other
cells in the central nervous system. Kuntz has also shown that
the cells of the sympathetic ganglia migrate to the periphery
largely from the dorsal root ganglia. They eventually form the
series of ganglia underlying the vertebral column. Two longi-
tudinal strands, the sympathetic trunks, connect the ganglia
with one another. Other sympathetic ganglia are found among
the viscera and in the head region, closely associated with the
cranial nerves. Sympathetic fibers, after making a synapse in
these ganglia, proceed peripherally, where they innervate for the
most part the same structures supplied by the parasympathetic
fibers. The sympathetic and parasympathetic fibers are antag-
onistic in their effects. The action of the first is to halt the peri-
staltic movements of the gut, to tighten the sphincters of the same,
and to increase the heart beat. The parasympathetic impulses
have an exactly opposite effect, and their normal functioning
insures proper digestion, respiration, and heart beat according
to the extent of vagus control. The responses of smooth
muscles and glands innervated by the autonomic system are far
more diffused, less localized than those of the skeletal muscles.
This is dependent on the number and arrangement of the neurons,
which permit the impulse from one preganglionic fiber to be
transmitted to several motor neurons in the autonomic system.

In mammals, when under extreme stress, such as is produced by
asphyxia physiologically, or danger psychologically, there is a
great increase of heart beat, very large rise of blood pressure, and
an increase in respiration. Much blood is sent from the intestines
and viscera to the muscles in general, so that skeletal response
is secured by well-nourished muscles. Further to fortify this
response, more sugar is released into the blood stream, and

R.B., renal branches of the sympathetic to the Miillerian duct; R.C., rami
communicantes; R.C.F., ramus communicans of the N. facialis with the pharyn-
geal nerve, R.C.V., ramus communicans of vagus nerve; Rec, rectum; R.Sub.,
subclavian ramus; S.Com., Stannius commissure connecting right and left chain;
S.K., sexual kidney; Sp.I., first spinal nerve; Sp.IX., ninth spinal nerve; Sp.X.,
tenth spinal nerve; St., stomach; V.C.A., vena cardinalis anterior; V.CaP., vena
cava posterior; V.CaP.X., vena cava posterior dissected; V.C.P., posterior cardi-
nal (rein; V.C.P.X.. posterior cut end of vena cava posterior. (After Andersson.)

374

THE BIOLOGY OF THE AMPHIBIA

intestinal movements are stopped or much decreased so that the
blood can be sent to the surface. Such a condition is evoked in
man by an emotional stress such as anger, rage, or fear (Cannon,
1915). The extent to which this complex of sympathetic defense
responses are organized in amphibians is not very clear, but as
bodily changes apparently occur under stress we may assume that
Amphibia experience emotions if only in a rudimentary form and
that the mechanisms evolved are probably basically the same.

References

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Cole, Elbert C, 1925: Anastomosing cells in the myenteric plexus of the
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Detwiler, S. R., 1927: Die Morphogenese des peripheren und zentralen
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and R. L. Carpenter, 1929: An experimental study of the mech-
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Durken, B., 1912: tiber friihzeitige Exstirpation von Extremitatenanlagen
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Gaupp, Ernst, 1899: "Ecker's und Wiedersheim's Anatomie des Frosches,"
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Hering, H. E., 1897: Uber Bewegungstorungen nach zentripetaler Lah-
mung, Arch. exy. Path. Pharm., XXXVIII, 266-283.

Herrick, C. Judson, 1914: The cerebellum of Necturus and other urodele
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, 1921a: The connections of the vomero-nasal nerve, accessory olfac-
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, 1924: The amphibian forebrain; I. Amblystoma, external form,

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, 1925: Amphibian forebrain; III. The optic tracts and centers of

Amblystoma and the frog, Jour. Corny. Neurol, XXXIX, 433-489.

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Kappers, C. U. A., and E. B. D. Fortuyn, 1921: " Vergleichende Anatomie

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376

THE BIOLOGY OF THE AMPHIBIA

Loeser, W., 1905: A study of the functions of the different parts of the frog's

brain, Jour. Comp. Neurol., XV, 355-373.
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Muchin, N., 1895: Die unipolare Reizung des verlangerten Markes des

Frosches, Zeitschr. Biol, XXXII, 29-48.
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Wirbeltiere, 5. Verh. Akad. Wet. Amsterdam, II Sekt., XVII, 1-23,

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Ten Cate, J., 1928: Contribution a la physiologie de la moelle epiniere
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reflexe; I. Versuche an Bufo vulgaris, Fol Neuro-biol, II, 718-729.

CHAPTER XVI

INSTINCT AND INTELLIGENCE

The evolution of the Amphibia is closely correlated with
changes in their habits. These habits may be either learned or
instinctive. As in the case of other animals, Amphibia develop
with certain combinations of neurons connected with sense
organs and muscles. It is the normal response of these inherited
patterns of neurons to certain sensory stimuli which is called an
' ' instinct. ' ' Not only the number and kind of reflex arcs involved
determines the nature of the response but also the time and
intensity relations of the nerve impulses arriving at the synapses
as well as the conductivity of the synapses at a particular moment.
As indicated in the preceding chapter, the internal state of an
organism may have a profound effect on permitting impulses to
pass from one neuron to another. Age, nutrition, hormones from
the gonads, pituitary, and other glands of internal secretion, the
osmotic condition of the body fluids, the amount of oxygen in
the blood, these and many other factors may influence behavior in
an amphibian by modifying the synaptic resistances. Internal
states may also shift the dominance of certain reflexes. Thus in
most animals the protective reflexes take precedence over other
reflexes, but in frogs during the breeding season, the clasping
reflex may take possession of the final common path and be
prepotent over the avoiding reflexes stimulated by noxious stimuli.

Although instinct involves a series of reflex arcs, it differs
from a reflex in more than its complexity. An important charac-
teristic of the instinct is the delay in its completion. A persistent
tendency toward some biological end is set up by a given stimulus
and this releases a series of responses directed toward a future
result which is finally attained. The mating instinct of the
newt leads through a long series of reflex responses on the part of
both sexes to the final deposition of the spermatophore by the
male and its taking up by the female. The possible habits which
an animal may possess are limited by its inherited nervous
organization and by the range of its modifiability during life.

377

378

THE BIOLOGY OF THE AMPHIBIA

The central nervous system of the Amphibia is so much simpler
than that of higher vertebrates, that it is surprising to find many

of the instinctive habits of the
higher forms already estab-
lished in the group, if only in a
rudimentary form. The ques-
tion of the origin of these in-
stincts and reflexes may be
considered first from the onto-
genetic side.

Development of Reflexes in
Ambystoma. — If the young
Ambystoma embryo is removed
from the egg capsule and tested
in regard to its reaction to
tactile stimulation, it will be
found to pass during develop-
ment through five stages which
Coghill (1929) has called the
' ' non-motile , " ' ' early-flexure , ' '
"coil," "S-reaction," and
"swimming stages." A light
touch on the skin brings no re-
sponse at first. Later the head
is moved away from the source
of stimulation. A little later
the bending involves more and
more of the trunk until the
embryo is thrown into a coil.
Still later, the flexure, which
begins in the head region and
progresses tailward, is reversed
in the head region before it has
passed entirely through the
trunk. Finally, this last reac-
tion is repeated at sufficient
intervals to effect locomotion.

Fig. 130. — A diagram of the neuro-
motor mechanism of swimming in
Ambystoma. The initial impulse, a,
passes tailward and excites the muscle
segments to a wave of contraction
which progresses tailward. The neu-
rons of the motor tract in the anterior
region develop collaterals which form
a synapse with the commissural cells
of the floor plate. Hence the impulse
also passes at b to the motor system of
the other side where it passes tailward, c,
inducing a second wave of contraction
which follows the first after a brief in-
terval. (After Coghill.)

Coghill has shown that the
anatomical basis of this orderly series of events lies in the growth
of nerves in medulla and spinal cord. Afferent neurons grow
across the motor tract of their own side of the cord at its anterior

INSTINCT AND INTELLIGENCE

379

end, to form synapses with commissural cells which convey
the excitation to the motor tract of the opposite side (Fig.
130). Impulses traveling these neurons induce a turning of the
head away from the source of stimulation. Reversed flexure
movements are caused by the excitation of sensory nerve endings
in the muscles on the side of contraction and by the conduction
of that excitation to the muscles of the opposite side. These
reversed flexures may lead to some locomotion but not to
typical swimming movements. It is apparently the growth
of motor fibers on the original side of stimulation which permits,
during the swimming stage, a contraction of the muscles of this
side. Since more synapses are involved in shunting the excitation
to the opposite side, the flexure away from the side of stimulation
follows the first flexure after a brief interval. During both the
S-reaction and the swimming stage the first flexure is the stimulus
for the second, and the second for the third. Experience and
exercise play no part in teaching Ambystoma how to swim.
Nerves grow because of their own potentialities, and the series
of different responses arise as new synapses are formed between
the nerve processes.

The reflexes of walking in Ambystoma are derived, as Coghill
(1929) has shown, from this swimming-reaction pattern. The
first motor nerves reaching the muscles of the limb are branches
of the same fibers that are stimulating the trunk muscles into
contraction. The first movements of the limb are, therefore,
correlated with body movements, and the limbs respond to pos-
tural stimulations earlier than to external influences. Walking
has not arisen by the coordination of local reflexes in the append-
ages. The arm is moved as a whole before the forearm gains
independent action, and the forearm develops its reflexes before
the digits acquire theirs. The basis of this development of local
reflexes within a larger pattern is the growing of collaterals from
already functioning nerves into new territory. The tongue of
Ambystoma receives branches from the motor neurons engaged
in integrating trunk movements long before the tongue has
muscle tissue in it (Coghill, 1929). Thus, adaptive movements
of tongue or limbs have not arisen by a coordination of local
reflexes which at the beginning had considerable independence.
Rather, reflexes arise by the individuation of portions of a larger
behavior pattern. During both ontogeny and phylogeny the
swimming movements of the trunk are reduced, while the limbs of

380

THE BIOLOGY OF THE AMPHIBIA

Amphibia acquire a greater independence of action. In sala-
manders the primitive sinuous movements of the trunk have not
been wholly given up in even the most efficient walkers.

Walking, just like swimming, is, therefore, native and
unlearned. Matthews and Detwiler (1926) reared Ambystoma
larvae 8 days in chloretone and found that at the end of this time
they had developed the same reflexes as in controls which had
been active during this period. The work has been extended to
Wood-frog tadpoles by Carmichael (1926) with similar results.
Carmichael (1927) has also repeated the experiments on Ambys-
toma larvae. He has found that the first observable response in
an individual reared in chloretone was on release from anaesthetic
essentially the same as in one that had been free-moving during
the same period of growth. It is from such observations as these
that we must conclude that " Nerve cells, like seeds planted by a
gardener, spring up and grow according to a definite pattern,"
and it is the position and interrelationships of the twigs of the
growing plant which give at various stages of development the
different behavior patterns to the organism which happens to
bear this sprouting seed. Walking, as well as swimming, is the
end result of nerve growth and adjustment. Experience has
nothing to do with the form into which the behavior of the animal
is cast.

Multiple Uses of Single Reflexes and Instincts. — It sometimes
happens that the same reflex may gain a different significance in
different groups of animals. For example, one of the most strik-
ing reflexes among Salientia is the so-called "unken" reflex.
The European Fire-bellied Toad, Bombina bombina, if suddenly
disturbed will bend its head and legs sharply back over the body
and turn the ventral surfaces of its forearms upward in such a way
that more or less of its gaudily colored undersurfaces are exposed
(Fig. 131). This habit also appears in the same form in the brightly
colored but unrelated Dendrophryniscus stelzneri (Fernandez,
1927) and has often been assumed to be a warning attitude on the
part of the toad, for its skin is more poisonous than that of various
other European Salientia. It is assumed that the toad's possible
enemies, if sufficiently warned, would avoid an encounter. Loh-
ner (1919) has found that the reflex may be evoked even in decapi-
tated animals and hence must have its coordinating centers in the
cord. The typical unken reflex is characterized not only by a
distinctive posture and immobility but also by a closure of the

INSTINCT AND INTELLIGENCE

381

eyes, a slowing down of the respiratory movements, and an
increase in the skin secretion. Though decapitated animals
assume the characteristic pose, the reflex is not present at its
maximum. Thus, the brain of the intact animal has some influ-
ence on this reflex. Whatever may be the significance of the
reflex in Bombina, Hinsche (1926) has shown that the same reflex
is present in the drab-colored Midwife Toad, Alytes, and, further,
that various European species of Rana and Bufo exhibit more or
less of the reaction. In these forms the reflex might be of assist-
ance in avoiding obstacles to locomotion. The Bullfrog, Rana
catesbeiana, if cornered, will sometimes thrust out its arms and
flatten its body. The back is not curved upward as in Bombina,
but otherwise the reaction has a considerable resemblance to the
unken reflex. At low temperatures the reflex of Bombina is

Fig. 131. — The "unken reflex" of Bombina bombina.

incomplete and resembles that of Rana, giving further evidence
that both reflexes have the same neuromuscular basis in spite of
the different functional significance in the two groups. The
reflex has also been compared with the induced state of tonic
immobility in animals and with hypnotism in man. Frogs
stroked on the back or laid ventral side up frequently "play
dead." The reaction is so different from the avoiding movements
of the unken reflex that the two phenomena would seem to have a
different nervous basis. Whether or not the unken reflex is a
type of tonic immobility, both types of response need not involve
the higher centers of the brain. If the back of a decerebrate frog
is rubbed, it exhibits the usual hypnotic response. Further, the
response is greater in the female than in the male (Verworn, 1897).
This response may have some significance in the mating process, a
vigorous grip of the male tending to throw the female into a state
of tonic immobility and thus prevent her escape.

The unken reflex is an example of stereotyped behavior com-
mon to a natural group of forms and yet modified according to the

382

THE BIOLOGY OF THE AMPHIBIA

species. Have all reflexes and instincts been gradually modified
in this way during phylogeny? In the ontogeny of Ambystoma,
Coghill showed that the growth of certain axons and dendrites a
fraction of a millimeter changed a helpless individual into one
capable of exploring its environment. Similarly, in phylogeny,
we should expect totally new behavior patterns to arise fully
formed as the result of small morphological changes of the nerve
patterns. Nevertheless, some reflexes and instincts have
remained relatively stable during evolution, while others, such as
the unken reflex, have been gradually modified. Since the walk-
ing reflexes have arisen from the swimming reflex pattern by
individuation of parts during ontogeny, the same phenomena of
individuation might be expected to account for the origin of new
reflex patterns from a more generalized behavior pattern during
phylogeny.

Defense Reaction. — One of the most complete studies of the
phylogenetic change in a behavior pattern in Amphibia has been

Fig. 132. — The defense-fight reaction of Bufo calamita. {After Hinsche.)

made by Hinsche (1928). Most Salientia when annoyed will
inflate their lungs and bow their heads, assuming a defensive
attitude. The inflation increases the size of the body and removes
all wrinkles from the skin. Smooth, swollen frogs are both
difficult to seize and difficult to swallow. Some toads add to
this defense reaction several aggresive movements. The limbs
are stretched, bringing the body clear from the ground, and then
the whole body is brought forward in a butting reaction (Fig. 132).
At the same time, the Spade-foot Toads may give a " fright cry,"
and frogs may scream with open mouths. Apparently, Cera-
tophrys and Leptobrachium carinense add effective biting move-
ments to this chain of reactions. There is no doubt that both
the defensive and offensive components of this series of events

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383

are effective in warding off the attacks of both snakes and birds.
The inflation of the body and the straightening of the limbs are
part of the defensive mechanism of lizards, and hence at least
this part of the response may be considered an ancient inheritance
from the early tetrapods.

The defense-fight reaction may be evoked in Salientia by either
optical or tactile stimulations. Hinsche found that color had no
modifying influence but that both the size and the speed of the
approaching object were important considerations. Small
objects elicited a feeding reaction in Bufo vulgaris, while objects
larger than 75 sq. cm., unless possessing projecting parts, induced
no response. Toads suddenly confronted by a mass of wriggling
worms lowered their heads and charged, but when the worms
began to disentangle themselves this defense-fight response was
replaced by the feeding reaction. By using the legless lizard,
Anguis, of different sizes, Hinsche was able to establish that
B. vulgaris would react to a moving wormlike creature of less than
23 cm. in length, chiefly by the feeding response, while similar
creatures above that size evoked principally the defense-fight
reaction. Large snakes were not effective as a whole but only in
so far as their head and tongue came within the requirements
necessary to induce the response. The sight of harmless animals,
such as rabbit and guinea pig, as well as of such objects as a rubber
tube, could call forth the response, while many enemies either
too large or too swift brought no reaction. The approaching
animal, in brief, is not received as an enemy but only as a bearer
of certain adequate stimuli. The defense-fight reactions of
Bufo are specific not to hostile enemies but to a complex of stim-
uli. Nevertheless the reaction was found to be effective against
the toad's greatest enemies, snakes, which were of sufficient size
and approached slowly enough to call forth the response. The
touch of a snake's tongue or head augmented the response
evoked by the sight of the snake.

Many factors modified the response of toads to possible
enemies. During states of maximal excitation all moving objects,
whatever the nature of the movement, were effective. Toads in
a corner responded more quickly with a defense-fight reaction
than those with avenues of escape open to them. The flight
response was in a certain sense antagonistic to the defense-fight
response. It was, perhaps, for this reason that frogs capable
of rapid flight failed to exhibit a complete defense-fight reaction

384

THE BIOLOGY OF THE AMPHIBIA

under laboratory conditions. In their phylogeny the flight
response had been developed to the detriment of the alternative
response. In the same way, natural selection may have pro-
vided that the snapping reflexes of Ceratophrys, a cannibalistic
form, were made part of the fight response rather than that they
remained a wholly separate reaction induced by the sight of
small moving objects as in the case of the toad.

The various components of the defense-fight reaction, although
linked closely in this response, are apparently used separately
under other circumstances. Thus the humping of the back with
the lowering of the head is used in skin shedding. The same
reflex helps the male to maintain his grip on the female, and
Hinsche finds the defense kicks used by embracing males to ward
off their competitors the same as the rearing reflexes in the
defense-fight response. In burrowing, the crouching and rearing
would also be effective. Similarly, the eye-closing reflex has
important functions other than those concerned with protecting
the eyes. In most Salientia and many urodeles the retraction of
the eyeballs aids in the swallowing, for the eyeballs are forced
partly into the mouth cavity and tend to carry the food toward
the midline and posteriorly. Hinsche (1926 b) has shown that
tactile stimulations of a limited part of the roof of the mouth
induces the reflex in the toad, and no doubt the pressure of food
on this area calls forth reflexly the retraction of the eyeballs.
Thus, reflexes, whether or not part of an original pattern, may be
used separately for totally different functions.

Even though the reflexes may be linked in certain patterns,
interfering reflexes or states of excitation must be absent before
any one complete chain of responses may be elicitated. Evolu-
tion has proceeded by the shunting in of new reflexes as well as
by a modification of the old. Species, such as Bufo calamita,
which are given short legs by heredity, are not able to exhibit the
same manifestations of the defense-fight reaction as longer-legged
species. The form of the animal, as well as its state of excitement
may both modify the response.

Phylogenetic Change of Instincts. — Many behavior patterns of
Amphibia exhibit phylogenetic changes. Such, for example,
may be seen in the courtship of salamanders. Here reflexes are
linked together as in the case of the defense-fight reaction, but a
longer interval occurs between the several responses. Courtship
behavior is, thus, a good example of an instinct, and the phylo-

INSTINCT AND INTELLIGENCE

385

Fig. 133. — The evolution of the courtship of some salamanders. A. Hydro-
mantes genei. B. Eurycea bislineata. C. Triturus viridescens. D. Euproctus
asper. (After Dahne.) E. Pleurodeles waltl. F. Ambystoma maculatum.
(After Breder.) G. Hynobius lichenatus. (After Sasaki.)

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THE BIOLOGY OF THE AMPHIBIA

genetic change of this instinct within a single group of Amphibia
may be considered in some detail (Fig. 133). The most primitive
urodeles living are the Hynobiidae. The males come first from
hibernation and resort to temporary pools, slow-moving streams,
and in a few instances to lakes. They are followed a day or so
later by the females, which soon begin to lay their paired sacs of
eggs. Sasaki (1924) has made detailed observations on Hynobius
lichenatus. The female selects a rock or other submerged object
and an attempt is made to glue the egg sacs to it. This is followed
by backward movements for the purpose of drawing the remainder
of the egg sacs out of the oviducts. The males, which up to this
point are indifferent to the females, now dart rapidly forward and
clutch the egg sacs with their forelimbs, while they push the
females away with the hind ones. The males rub the egg sacs
with their cloacal lips while fertilizing them, and the movements
of their hind limbs assist in the delivery of the eggs. The males
still cling to the eggs for a period after the female has deposited
the spawn and has sought concealment under some object.

The Cryptobranchidae may be considered permanent hynobiid
larvae or partly metamorphosed forms of large size. Although
living throughout the year in the water, they become gregarious
during the breeding season, which occurs in the fall, as with some
specimens of H. lichenatus. Fertilization is external as in the
Hynobiidae, and the sight of the string of eggs seems to be the
immediate stimulus for the emission of the sperm (Smith, 1907).
The tendency for the male hynobiids to remain with the eggs is
extended in the cryptobranchids, for here the males stay with
them until hatching and may frequently devour part of their
trust.

The ambystomids show a close relationship to the hynobiids,
but they have developed a true courtship which can be evolved
only with difficulty from the pattern of the hynobiids and
cryptobranchids. The males precede the females to the pond
and, in Amby stoma maculatum at least, engage in a Liebesspiel
on the appearance of the females. The males twine back and
forth over one another and rub their snouts against each other's
tail or body, beginning usually at a posterior point and working
forward, the most aggressive male frequently pushing his head
under the body of another. In the axolotl, according to Gasco
(1881), both sexes take part in these caressing movements.
Wright and Allen (1909) found that the mere presence of the

INSTINCT AND INTELLIGENCE

387

female in the jar with males excited them to sexual activity, but
whether the males could sense the eggs in the body of the female
or were stimulated by some other factor was not determined.
The female axolotl noses the cloaca of the male, apparently
attracted by the secretion of the abdominal gland. Males of
this and other species of Ambystoma have been found to fan their
tails in the direction of the female during courtship, apparently
to waft the same secretion toward her. The male of one species
of the genus, A. jeffersonianum, apparently seizes the female with
his hind legs (Wright, 1908). In brief, there occur in Ambys-
toma elaborate rubbing movements directed toward the females,
and apparently it is the secretions released by the male which
hold her interest. The nature of the sensory stimulations which
first arouse the interest of the male in the female is unknown.
The courtship of Ambystoma is directed toward stimulating the
female to the point where she will pick up the spermatophore
which the male deposits. Gasco (1881) describes the female
axolotl as pressing the spermatophore into her cloaca with her
hind limbs, but in A. maculatum the cloacal lips take up the sper-
matophore unaided. Fertilization is internal, the males taking
no interest in the eggs which are laid several days or more after
impregnation.

The courtship of all the other families of salamanders, as far
as known, seems to have been built out of the pattern of Ambys-
toma by the elaboration of one or more phases of it. The
primitive salamandrids Tylototriton, Pleurodeles, and Sala-
mandra have given up the random rubbing movements and
elaborate further one reaction found in Ambystoma. The male
creeps under the female and seizes her front legs from behind,
with his front legs. The " piggy-back ride" which follows finally
results in the emission of the spermatophore by the male and its
being secured by the female. This peculiar courtship, which
may occur either on land or in water according to the species, is
probably found in other salamandrids such as Chioglossa (Bou-
lenger, 1910), but it does not occur outside the family. In some
species more or less of the nosing and cloacal display also occurs.
A few primitive salamandrids have seized upon other phases of
the courtship seen in Ambystoma and developed them along
other channels. Klinge (1915) reports the male Triturus pyrrho-
gaMer, a Japanese newt, as partly gripping the female from above
with both pairs of limbs while lashing with his tail to drive secre-

388

THE BIOLOGY OF THE AMPHIBIA

tions of the cloaca toward her. One forelimb is placed over her
neck and one hind limb across her back to hold her while the
cloacal secretion is wafted toward her. After the spermatophore
is deposited and the female has brought her cloaca in contact
with it, the male may bite the female in the inguinal region and
this is said to aid in the taking up of the spermatophore (Klingel-
hoffer, 1930).

The western newt of America, T. torosus, is probably closely
related to T. pyrrhog 'aster, and its courtship is essentially the
same. The male grips the female with fore- (Schreitmuller, 1909)
or both pairs of limbs (Storer, 1925). The eastern newt, T.
viridescens, uses its hind limbs for the same purpose and brings
its cheek against the snout of the female. The cheek is equipped
with a battery of hedonic glands which serve to quiet the female
(Rogoff, 1927) and finally to induce her to follow the male while
he moves off a short distance and emits the spermatophore. It
is probable that similar hedonic glands are found in the tail
spine of Salamandra caucasica, but their functioning has never
been observed. Schlosser's account (1925) of the courtship of
Salamandra atra suggests that hedonic glands may function in
this species as well. Apparently the male seizes the female
about the neck with his forelimbs and rubs some of his secretion
into her nostrils. Whether S. atra also carries the female in a
preliminary " piggy-back ride" as in S. salamandra is not known,
for a complete courtship of the species has not been witnessed.

The European newts of the genus Triturus represent anatomi-
cally a more advanced group of salamandrids than the species
just mentioned. They have developed still another mode of
interesting the female in the business of picking up the sperma-
tophore. The males are for the most part conspicuously colored
and they display themselves before the female. Sexual dimor-
phism of color is found also in T. pyrrhog 'aster , the female having
a red stripe on the tail, the male a black one. This difference
may help the clutching males to distinguish females from their
own sex, but the dark tail is not used in display. The nosing
and tail lashing movements of Ambystoma also occur in the Euro-
pean newts.

Strotgen (1927) saw the diminutive Salamandrina deposit
spermatophores. Since the male was following the female, the
courtship may resemble that of Ambystoma. The mountain
newts of Europe, Euproctus, are not conspicuously colored,

INSTINCT AND INTELLIGENCE

389

and since they live in mountain streams or near the bottom of
lakes, they have little opportunity for display. They, on the
other hand, seem to have elaborated the entwining phase of
the courtship of Ambystoma. The males lie in wait for the
female and seize her with either tail or teeth. The fore- or hind
limbs are also used, according to the species, to maintain the
grip. The spermatophore may be either deposited near the
cloaca of the female or transmitted directly into it. In brief,
various natural groups of genera or species of salamandrids are
each characterized by its own distinctive type of courtship, the
most essential features of which seem to be a further specializa-
tion of part of the courtship exhibited by Ambystoma. The
Salamandridae probably did not evolve directly from ambys-
tomids, but both may have evolved from the same stock. It
would seem that this stock exhibited a generalized type of court-
ship which was retained by Ambystoma, but parts of it were
modified in different ways by the various natural groups of
salamandrids.

The Plethodontidae, which evolved directly from salamandrids,
seem to have specialized in hedonic glands as the source of stimu-
lation. While these glands are restricted to the cheek of the
newt and apparently the tail of Salamandra caucasica, they are
widely distributed over cheeks, body, and tail of most male
plethodontids. Their courtship was first made known in Eurycea
bislineata. The male noses the female and frequently bends his
head across her cheek exactly as in the case of the newt in
amplexus. The female finally shows an interest in him and steps
across his tail to press her snout tightly against the glands in his
tail base. The pair then engage in a grotesque walk, the male
bending his tail sharply at the base. Other plethodontids, as
shown by Noble and Brady (1930), may differ from Eurycea in
certain details of the first phase of the courtship. It is interesting
that the "tail walk" should proceed in exactly the same manner
in both the aquatic Eurycea and the terrestrial Hemidactylium,
although possibly lost in Hydromantes. The character of the
medium, thus, fails to modify the courtship pattern in both sala-
mandrids and plethodontids. The courtship pattern would seem
to have evolved in phylogeny without a close habitat correlation.

It would appear that any behavior as complex as the courtship
of Salamandra or Eurycea, and involving the two sexes for its
successful conclusion, must have some psychical content. The

390

THE BIOLOGY OF THE AMPHIBIA

development of specialized courtships out of a more general
pattern tends to keep the derived groups from ever crossing.
Even if the germ cells could be cross-fertilized, no interbreeding
would occur in nature, for the groups would not be psychically,
that is, instinctively compatible. Within any one group of
related species there appear to be other mechanisms which
prevent crossing. Thus, Noble and Brady found that Stereo-
chilus and Eurycea would not court with one another. Since
the males nosed the females before rejecting them, there was
apparently some odor in the skin of the females which was dis-
tasteful to the males.

Mechanism of Instinct. — Although the courtship of many
salamanders has a very stereotyped form, the centers in the cen-
tral nervous system controlling this or any other instinct have
never been determined. Each instinct probably embraces a
great many centers. As suggested by the breeding of Eurycea,
one center aroused by an initial stimulation makes possible the
activation of a second center by a different type of sensory
impulse from that which aroused the first center. Various
instincts such as the hunting reaction may be induced by impulses
from visceral centers. Instincts are, therefore, internal states of
readiness which exist until the proper stimulus releases the cul-
minating reflexes. In the hunting reaction the stimulus would be
the sight of food, and the culminating reaction the snapping and
swallowing reflexes. During the breeding season, the hormones
from the gonads make possible the functioning of certain reflexes
such as the clasping reaction, but the mating instinct is not
satisfied until a series of reflexes have functioned, more or less in
their proper order.

The unfolding of an instinct such as that of hunting discloses
that one stimulus and response may predispose a second reflex
to function. Further, Amphibia differ in the degree to which
they "warm up" to a situation. For example, Yerkes (1905)
found that if a sound was produced near a frog within two seconds
of the time of a tactile stimulation, the response to the latter was
greater than if there was no sound. If the sound came over 2
seconds before the tactile stimulus, it had no " significance" for
the frog; that is, the response was not affected. Bruyn and Van
Nifterik (1920) found in the toad that even with an interval of
10 seconds between noise and tactile stimulus there was still a
great reinforcement of the reaction. Sound has thus a much

INSTINCT AND INTELLIGENCE

391

greater significance for toad than for frog. Once an insect has
given away its location by a sound, the toad is " tuned up" and
holds this tuning much longer than the frog. The toad is thus
better equipped to hunt than the frog. Although neither frogs
nor toads respond to ordinary sounds by movement, toads have a
greater power of retention than frogs, and this persisting nervous
state makes them better fitted to survive competition on land.

Thus, a nerve center such as the acoustic nuclei in toads does
not always discharge instantly into a motor tract. It remains
pent up, predisposing a second center, over which it has no motor
control, to function more effectively when the proper external
stimulus arrives. Worms which were writhing too violently, due
to the fact that they were fastened to a pin, did not induce the
feeding reactions of Bufo calamita, according to the observations
of Franz, so quickly as did normal worms. Many Amphibia
make use of certain stimuli to put them on guard when hunting,
and other excitations to release the snapping reflexes. Thus,
salamander larvae turn their heads toward forceps thrust in their
aquaria, for they feel the vibrations with their lateral-line organs.
When these stimulations are reinforced by olfactory or optic
impulses, the snapping reflex is finally evoked. Whitman (1899)
has shown that a similar cautious approach toward possible
food is employed by both young and old Necturus. The adults
are very successful in capturing living prey, merely because they
have inherited a nervous organization which demands delibera-
tion or warming up before the final attack. Instincts may in
some cases take as good care of an organism as intelligence in the
same circumstance could do.

If the vibratory stimulations impinging on a Necturus should
be excessive, they would evoke not approach, but flight move-
ments in the animal. One cutaneous area can produce different
reflexes according to the quality or nature of the applied excita-
tion. Detrimental stimulations evoke defense or preservation
reflexes, while useful excitations call out other movements which
are usually opposed. This is well shown by Ten Cate's experi-
ments (1928) on locomotion in the newt. A gentle stimulation
of the soles of the hind feet after the spinal cord has been cut
brought forth walking movements; a stronger stimulation of the
same area released defense reactions. The modifying influence
of a reflex might come through the central nervous system from
another center. Thus, unusual visual impressions in either

392

THE BIOLOGY OF THE AMPHIBIA

Necturus or the newt might evoke flight movements of the
limbs instead of an approach. Such behavior need not possess
any psychical content. If a frog with its brain entirely destroyed
is slightly pinched on one foot, it will withdraw this appendage;
a stronger pinch evokes kicking reflexes; a more violent pinch
produces jumping movements. Obviously here the increased
stimulation has brought additional efferent paths into the reflex.
The higher centers of the brain may in the same way increase or
decrease the number of arcs involved whether or not these impul-
ses from higher up also have some psychical qualities. The
higher nerve centers of the brain thus inhibit or facilitate the
activities of the various reflex arcs of the spinal cord. Typical
reflex responses to definite stimuli occur more uniformly after the
brain has been destroyed than before.

Learned Behavior. — Although instinct is unlearned behavior,
it may, like most other inherited features of an organism, be
modified by environmental influences. The more loosely organ-
ized an instinct is the more chance there is for trial and error, and
this in turn allows experience to modify the pattern in favor of
one reaction instead of another. Learning is due to the increased
conductivity of certain neural paths. As discussed in the pre-
ceding chapter, the change apparently occurs at the synapses of
much used neurons. In all vertebrates the forebrain, especially
the cerebral cortex, contains the neural pathways which are most
subject to modification through use; in other words, these neurons
form the center of associative memory. Burnett (1912) has
experimented with decerebrate frogs. He found that in learning
a maze, the normal frogs of the species he used (R. pipiens and
R. boylii) would make their escape after about 20 trials with
rarely an error. For the decerebrate frogs over 100 trials were
made and the last trial was no more successful than the first.
Further, the reflex excitability of the decerebrate frog is height-
ened, owing to the loss of inhibitory influences from the higher
centers. Burnett concluded that the decerebrate frog is incap-
able of forming even the simplest associations. Hence, in
Amphibia as in other vertebrates, the forebrain must be con-
sidered the primary seat of learning.

Although all animals are able to learn, that is, to modify their
inherited reactions, it is not until the development of a cortex in
the cerebral hemispheres of higher vertebrates that a type of brain
is evolved which makes possible numerous juxtapositions of

INSTINCT AND INTELLIGENCE

393

sensory data and also gives the possibility that training may
influence to a considerable degree the effector path selected.
Such a brain is less stereotyped but more adaptable than the brain
of lower forms with their closely knit set of instincts. Hence, in
a changing environment it would surely succeed, while the latter
might fail to find an environment sufficiently stimulating to
release its highly organized chains of reflexes.

Amphibia, in spite of their rudimentary or lacking cortex, are
able to learn other things besides running mazes. As everyone
knows who has kept salamanders or frogs for any length of time
in aquaria, most regularly fed Amphibia soon learn the source
of their food and expectingly turn their heads when anyone
approaches their tank. Toads fed only once a week learned the
feeding time after only 30 or 40 feedings and displayed distinctive
reactions on these occasions even before the food was presented
(Vandel, 1927). Schaeffer (1911) found that three common
species of Rana learned to avoid disagreeable objects such as
hairy caterpillars in from four to seven trials. This learned
habit persisted for at least 10 days. When assisted by the
punishment of an electric shock, a Pond Frog learned to avoid
earthworms treated with chemicals in only two trials. Buyten-
dijk (1918) found that two European species of toad would
seize red ants, Formica rufa, but after a single experience would
avoid not only an ant but even spiders and flies. The following
day ants were avoided but spiders were taken. Rarely, a toad
would seize an ant on the second day, but usually it was not
until the third or fourth day after the capture of the first ant that
others were taken. Thus, toads may learn as quickly as mam-
mals, but they remember for only a limited period. Razwilowska
(1927) taught a frog to associate a square of a certain size with
food. When only the square was presented, the frog reacted as
if food were present. This is the more surprising in that Franz
(1927) showed that even after feeding Rana temporaria and Bufo
calamita for months with meal worms, they would respond only
to moving, never to the quiescent, objects. A meal worm had
no "significance" for these Amphibia unless it moved. Buyten-
dijk (1918) found that a toad may seize a moving piece of paper
but after one experience will not make a second attempt for some
minutes. If, however, the toad is fed an insect, it will return to
the attack on the paper. Experience thus changes the signifi-
cance of an object. A single successful capture of an insect

394

THE BIOLOGY OF THE AMPHIBIA

modifies the reaction of the toad toward another object. It
changes the toad's " point of view."

Any object in a stable environment has a different significance
for Amphibia at different times. This significance varies not
only with experience but also with the physiological state of the
animal. Haecker (1912) found that axolotls could be taught to
distinguish between a piece of meat and one of wood of the same
size. During the breeding season the number of errors in making

Fig. 134. — Glass plate experiment with Bufo calamita. The position of
the glass plate and the path selected by the toad are indicated for successive
trials. {After Buytendijk.)

this distinction increased. Flower (1927) found that axolotls
during metamorphosis completely forgot earlier feeding experi-
ences and had to be taught all over again. Sexual activity and
metamorphosis may thus affect the learned behavior. No
doubt hunger, noise, and other stimulations would also have an
effect on learned behavior, whether or not acting directly on the
reflexes.

Amphibia show some aptitude in learning motor habits.
Terrestrial forms such as toads and newts learn to find their way

INSTINCT AND INTELLIGENCE

395

through a maze more quickly than aquatic species as the frog.
Buytendijk (1918a) showed that toads in seeking for obscurity
will learn after only nine trials how to avoid a glass plate placed
directly in their way. Buytendijk found, as Cummings (1910)
had observed in a British newt, that movements once made
tended to be repeated in later trials (Fig. 134). Motor reactions
which are not harmful or which do not conflict with some bene-
ficial activity tend to persist. This " muscular memory" is
doubtless of assistance in helping toads find their way back to
their usual retreat after a night of hunting. Buytendijk found
that useless motor habits not only persisted a long time in the
toads he studied but could even reappear with more or less
modification after they had once disappeared.

Homing is not accomplished entirely by muscular memory.
As Franz (1927) showed with toads, vision plays an important
role in controlling the orientation. Rana has not so good eye-
sight as Bufo, and Franz showed that it found its way back to an
accustomed retreat with greater difficulty. The observations
of Yerkes (1903) make it clear, however, that vision plays a part
in the homing of Rana clamitans (Chap. XVII).

Intelligence. — In comparing toads with frogs, the former were
found not only to learn more quickly but to react more promptly
to many stimulations. Toads have, therefore, a greater intelli-
gence than frogs, for intelligence is not measured merely by
ability to learn. Responsiveness, curiosity, and persistence are
factors entering into the intelligence of toads and other verte-
brates. Franz (1927) concluded that Bufo calamita in its prompt
handling of complex food situations was on the same psychological
plane as reptiles. It is doubtful if Bufo, placed in the water,
the home territory of Rana, would prove as much a master of the
situation as the frog. Nevertheless, Hinsche (1926a) showed
that if the toad was gradually conditioned to the water it would
voluntarily return to it. Under these conditions, the toad
developed Rana-like movements which it never ordinarily dis-
closes. Apparently the aquatic environment permitted the
functioning of reflexes which usually do not appear during the
life of the toad. If Hinsche's interpretation is correct, other
Amphibia also may well have instincts and reflexes which they
never exhibit, merely because the conditions of their present
life do not activate them. The voluntary return to the water
induced by Hinsche may be compared with the normal migration

396

THE BIOLOGY OF THE AMPHIBIA

to the ponds in the spring. Apparently an environmental factor
can release an instinct in the toad, usually activated only by
secretions from the gonads.

It is highly probable that other Salientia are as intelligent and
as versatile as the toad. Biederman (1927) reports the European
Tree Toad as having a retentive memory, and Yerkes (1903)
found that the Pond Frog, Rana clamitans, could remember its
way out of a maze after the lapse of a month. The various
European Salientia differ greatly in their speed of learning and
ability to remember. Nevertheless, the Amphibia as a group are
not better endowed with ability to learn and to remember than
some fish (Hempelmann, 1926) . Learning seems to have plaj^ed
only a minor part in the success of the various groups of Amphibia.
The instinct patterns are so much more in evidence than learned
behavior throughout all groups of Amphibia, that the latter type
of behavior may well be neglected in considering the evolution of
the groups.

References

Biederman, S., 1927: Le sens et la memoire des formes d'un objet chez
les anoures; L'inversion de l'habitudes apres ou sans amortissement
(L'experience optique des Batraciens, He memoire), Prace. Inst.
Nenck., No. 56, 1-5.

Boulenger, G. A., 1910: " Les batraciens et principalement ceux d'Europe,"
Paris.

Bruyn, E. M. M., and C. H. M. Van Nifterick, 1920: Influence du son
sur le reaction d'une excitation tactile chez les grenouilles et les crapauds,
Arch. Neer. Physiol. Horn. Anim., Ser. IIIc, V, 363-379.

Burnett, T. C, 1912: Some observations on decerebrate frogs with especial
reference to the formation of associations, Amer. Jour. Physiol., XXX,
80-87.

Buytendijk, F. J. J., 1918: L'instinct d'alimentation et l'experience chez
les crapauds, Arch. Neer Physiol. Horn. Anim., Ser. IIIc, II, 217-228.

, 1918a: Instinct de la recherche du nid et experience chez les crapauds

(Bufo vulgaris et Bufo calamita), Arch. Neer. Physiol. Horn. Anim.,
Ser. IIIc, II, 1-50.

Carmichael, L., 1926: The development of behavior in vertebrates experi-
mentally removed from the influence of external stimulation, Psych.
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, 1927: A further study of the development of behavior in vertebrates

experimentally removed from the influence of external stimulation,
Psych. Rev., XXXIV, 34-47.

Coghill, G. E., 1929: "Anatomy and the Problem of Behavior," New York.

Cummings, B. F., 1910: The formation of useless habits in two British
newts (Molge cristata, Laur, and M. palmata, Schneid.), with observa-
tions on their general behavior, Zoologist, XIV, 161-175, 211-222, 272.

INSTINCT AND INTELLIGENCE

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Fernandez, Kati, 1927: Sobre la biologia y reproducci6n de batracios
Argentinos (Segunda parte), Bol Acad. Nac. Cienc. Cordoba, XXIX,
271-328.

Flower, S. S., 1927: Loss of memory accompanying metamorphosis in

amphibians, Proc. Zool. Soc, Part I, 155-156.
Franz, V., 1927: Zur tierpsychologischen Stellung von Rana temporaria

und Bufo calamita, Biol. Zentralbl., XLVII, 1-12.
Gasco, F., 1881: Les amours des axolotls, Zool. Am., IV, 313-316, 329-340.
Haecker, V., 1912: tjber Lernversuche bei Axolotln, Arch. ges. Psychol.,

XXV, 1-35.

Hempelmann, Friedrich, 1926: "Tierpsychologie vom Standpunkte des
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Hinsche, G., 1926: Vergleichende Untersuchungen zum sogenannten

Unkenreflex, Biol. Zentralbl, XLVI, 296-305.
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XLIII, 252-260.

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vulgaris und einige seiner Beziehungen zu anderen Reaktionen, Biol.
Zentralbl, XLVI, 742-747.

, 1928: Kampfreaktionen bei einheimischen Anuren, Biol. Zentralbl,

XLVIII, 577-616.

Klinge, W., 1915: Triton pyrrhogaster, Wochenschr. Aquar.-Terrar.-Kde.,
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Lohner, L., 1919: tlber einen eigentumlichen Reflex der Feuerunken,

Arch. ges. Physiol, CLXXIV, 324-351.
Matthews, S. A., and S. R. Detwiler, 1926: The reactions of Amblystoma

embryos following prolonged treatment with chloretone, Jour. Exp.

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Rogoff, J. L., 1927: The hedonic glands of Triturus viridescens; a structural

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propagates like the axolotl, Jour. Coll. Agric. Hok. Imp. Univ., XV,

Part I, 1-36.

Schaeffer, Asa A., 1911: Habit formation in frogs, Jour. Anim. Behav., I,
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Kde., XXXVI, 222.
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THE BIOLOGY OF THE AMPHIBIA

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Bldtt. Aquar.-Terrar.-Kde., XXXVIII, 94-95.
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XV, 279-304.

CHAPTER XVII

THE WAYS OF AMPHIBIA

The behavior of Amphibia has been briefly analyzed in the
previous chapter, but little space has been given to the placing
of these behavior patterns in their natural surroundings. Since
Amphibia learn little during their life, it is chiefly their instincts
which direct their movements. A few of the major activities
of Amphibia may be discussed in relation to their natural setting.

Migration. — Frogs, toads, and salamanders undergo periodic
migrations. There is such a close resemblance between these
migrations and those of fishes and birds that the causes and
controlling factors are apparently much the same. In the spring
most northern Amphibia come to the ponds or streams to breed,
the males usually preceding the females by one or more days.
This order of arrival at the breeding grounds occurs also in the
purely aquatic Megalobatrachus (Tago, 1929) and is character-
istic of many other groups of vertebrates. As with birds, the
male frogs and toads select calling stations and endeavor to
attract females toward them by their cries (Fig. 135). With sala-
manders, voice plays no part in either migration or sex recogni-
tion, and hence the early appearance of the males has no obvious
advantage. In correlation with the absence of voice the process
of successful mating is much more complicated in salamanders
than in frogs.

The problem of the causes of migration has two different
aspects: first, the development of a sensitivity toward certain
external stimuli, and, second, the nature of the directing mecha-
nism of migration activated by this change. The first process
is primarily controlled in Amphibia by the seasonal hypertrophy
of the gonads, which in turn are under hormonal control, espe-
cially by the anterior pituitary gland. Sexually immature indi-
viduals do not take part in the chief migrations. The final
releasing factor of the migratory impulse is a climatic change.
Wright (1914) showed the close correlation between the migration
of certain frogs of northeastern United States and the land or

399

400

THE BIOLOGY OF THE AMPHIBIA

water temperatures of the region, while others have stressed the
importance of a sudden increase of humidity in producing the
spring movements (Cummins, 1920; Noble and Noble, 1923).
Heavy spring showers usually initiate the migration of salaman-
ders of both local and foreign species (Kunitomo, 1910). In the
tropics, cooling thunderstorms of the wet season bring forth
thousands of loudly calling frogs. Bles (1906) showed the
importance of a slight cooling of the water in stimulating the
breeding activities of African water frogs, Xenopus. Frogs are
as sensitive to changes of temperature as are human beings
(Babak, 1912), and laboratory experiments have shown that
salamanders distinguish between regions of different humidities

Fig. 135. — The vocal pouch of Scaphiopus holbrookii. E., Eustachian tube; O.,
left orifice to pouch.

(Shelf ord, 1914). In addition to temperature and rain, local
conditions may affect the migrations of a species. Thus, Piersol
(1929) has shown that Ambystoma maculatum of a certain region
near Toronto deposited its eggs over an extended season with the
maxima about 10 days apart. This was due to the fact that the
adults hibernated in two banks which were unequally exposed
to the sun.

Nevertheless, Amphibia do not always show a close correlation
between migration and certain temperature and humidity levels.
Storer (1925) found that various western toads and frogs had a
protracted breeding season, and other species exhibited a certain
correlation between egg laying and times of flood. Migration
may in certain cases take place without any external stimulation,
for salamanders which are bred in the laboratory frequently
retain for a time a periodicity in their egg laying and probably,

THE WAYS OF AMPHIBIA

401

therefore, in their desire to migrate. Toads which were allowed
to hibernate in the laboratory at room temperature have been
known to appear in the spring at the right season and to call
loudly for mates before making an effort to find food or water.
It is highly probable that the migrations of many Amphibia are
controlled by such rhythms which are in turn determined by
climatic changes of previous seasons. These rhythms as sug-
gested by recent endocrine studies are directly controlled by
hormones released from the anterior lobe of the pituitary. Both
frogs and salamanders may be induced to lay their eggs out of
season by treating them with fresh anterior pituitary substance
(Chap. XIII). The release of this hormone from the pituitary
gland is probably under nervous control. This would account
for the close correlation of breeding with certain favorable
climatic conditions. Under laboratory conditions, certain spe-
cies, such as Pleurodeles waltl, may be induced to lay their eggs
merely by placing them in an ice box over night and trans-
ferring them the next morning to tanks suitable for breeding.
The sudden rise in temperature releases the ovulation cycle, and
both courtship and breeding will frequently follow.

Direction of Migration. — The second problem of migration is
the nature of the directing mechanism. This is probably not a
simple tropistic phenomenon, for Amphibia breed in a great
variety of situations, each species usually in a distinctive habitat.
Many land species migrate to ponds to breed, others to mountain
streams (Salamandra, etc.); some species move from trees to the
ground (some Eleutherodactylus) or from trees to bushes over
the water (Phyllomedusa) . Parker found that the migration
of the young Loggerhead Turtle into the sea was not controlled
by any stimulus received from the water. It was due in part
to a positive geotropic response and in part to a peculiar photo-
tropic response in that the animal responded to a detail of its
retinal image and moved always in the direction of a clear
and open horizon. Czeloth (1930) has attempted by laboratory
and field study to determine the kind of sensory data which
direct the annual migrations of European newts to and from the
ponds. He finds that both aquatic and terrestrial individ-
uals will follow the odors of garden earth or of decayed wood.
Although newts are able to sense and move toward damp situa-
tions, their response to earthy odors is stronger. Individuals
freshly removed from the water exhibit a marked positive geo-

402

THE BIOLOGY OF THE AMPHIBIA

tropism but eventually orient themselves in the direction of the
water and will move up and down inclines to reach it. In such
cases the newts may be responding to either moisture gradients
or odors of water vegetation. In the fall other kinds of sensory
data may prove more attractive. At this time of year the tend-
ency of newts to seek cover may extend to their directing them-
selves toward any object, such as a wood, which tends to darken
portions of the horizon. The European Salamandra responds
apparently much more specificially to environmental factors in
the fall, because at this season great numbers of individuals
seek the same retreat and form inpressive aggregations during
hibernation.

It sometimes happens that in birds and fishes the breeding
site may correspond to the probable home of the migrants'
ancestors. In another chapter it is pointed out that the breeding
habits of Amphibia frequently change more slowly than the adult
characters of a form. If a species retains the same breeding
habits of an ancestral form, it will tend to migrate to the same
breeding grounds. Thus, in Amphibia the derived species may
migrate to the ancestral home to lay its eggs. The mountain
salamander, Desmognathus fuscus carolinensis, returns to the
proximity of mountain streams and lays its eggs in the same man-
ner as its close relative D. f. fuscus which never lives far away
from the water. In cases, however, where the mode of life history
has changed, the breeding habitat may give no clue as to the cen-
ter of dispersal of a group. For example, Hemidactylium seems
to have been derived from the terrestrial Plethodon, but its
mode of life history is such that the species is forced to make
annual migrations to the borders of ponds.

The phenomenon of migration, or at least of the spring migra-
tion, may be considered a secondary sexual character found in
both sexes. The problem of migration is to determine, first, the
sensory mechanisms directing the movements and, second,
how the sex hormones elaborate or activate these mechanisms
and especially their central connections. In the discussion
of the secondary sexual characters it was pointed out that various
structures may appear during the breeding season and owe their
development to the presence of gonad hormones released at this
time. There are probably no special sense organs developed in
the breeding season to direct migration, but existing perceptual
mechanisms are especially sensitized by the sex hormones and

THE WAYS OF AMPHIBIA

403

then suddenly called into action by an external stimulus, a cli-
matic change.

A comparison may be made between the migration of the
young and of adult Amphibia. During metamorphosis there
is a great increase in metabolism and a need for oxygen. It
would seem to be primarily this factor which drives the metamor-
phosing Amphibia to land. It is known that the metabolism of
adult Amphibia changes during the breeding season, but no
marked drying of the skin or other bodily change has been
noticed which would account for the migration of the adults in
the reverse direction. The animals react to certain stimuli
which did not interest them at other seasons. If the olfactory
sense plays such an important role in migration as Czeloth's
work (1930) seems to indicate, some correlation between the
direction of the wind and the direction of migration would be
expected. Naturalists have often noted that the spring migra-
tions of Amphibia frequently follow definite routes, but they
have not correlated these routes with air currents. The reverse
migration away from the grounds after the breeding reflexes have
been released is, as would be expected, a far more haphazard
affair. In the case of the western Spade-foot Toad, Scaphiopus
hammondi, Goldsmith (1926) showed that while at first the adults
tended to move away from the pools, making 60 to 150 meters a
night along the drainage lines, the migrants after one or two nights
of rapid centrifugal movement spread out and moved more or less
at random. Czeloth (1930) found, however, that immature newts
captured in the act of migration from the ponds regained their
original orientation when released. In general, nevertheless,
when the breeding instinct is aroused, species react to certain sen-
sory data in a more or less reflex manner; while after the final re-
flexes have been completed, the species return to their usual
manner of living. Since the sensory and neuromotor mechanisms
of the various species are unlike, different breeding sites are
selected and competition is avoided.

The " homing instinct" is frequently brought forward in dis-
cussions of migration in other vertebrates. This ability to find
one's way home is not well marked in some salamanders (Cum-
mings, 1912; Storer, 1925), but the species which perform the
longest migrations have not been investigated in this regard.
Amphibia when they become sexually mature return to the type
of breeding site characteristic of the species and hence learning

404

THE BIOLOGY OF THE AMPHIBIA

could play no part during the first breeding season. It seems that
homing has little to do with the phenomenon of migration.

Although several kinds of sensory data are used by Amphibia
during their migrations, one of the most important in frogs and
toads would seem to be the voices of other males of the same spe-
cies. The first males which happen to reach suitable breeding
grounds begin to call. Other males and later females are
attracted by the sounds to the same vicinity. In this way three
or four species may be found breeding in colonies along the same
lake without any overlapping of breeding territory (Noble and
Noble, 1923). In frogs as in birds, the breeding territory is
usually marked out by the males, and voice in both seems to
alter or direct the migration route, or at least the path of the
individual, on nearing the breeding site.

Homing. — Laboratory experiments have demonstrated that
frogs, toads, and salamanders are able to learn how to find their
way through a labyrinth to an accustomed spot. In the case
of frogs and toads, it would seem that the animals are attuned to a
certain number of visual impressions and that new scenes are
avoided apparently because of discordant feelings which they
arouse. Since useless movements frequently reappear in succes-
sive trials, it would seem that Amphibia have also a " muscle
memory," at least for short distances. This obligates them to
repeat the same kind and number of movements on each return
home after one or more successful performances.

Field observations have demonstrated that Salientia make
frequent use of their homing ability whatever may be the nature
of their sensory impressions. Toads regularly return to the same
shelter at night. The large South American frog Leptodactylus
pentadactylus may have well-marked dens. During the breeding
season many tree frogs which hide during the day will return to
precisely the same calling station every night. This is especially
noticeable when the calling station is on an exposed portion of an
isolated limb. Breder (1925) found that the males of Hyla
rosenbergi, in Panama, returned on successive nights to the mud
basins they had constructed along the stream bed for the care of
their eggs and tadpoles.

Franz (1927) found that frogs could not home so well as
toads, but I have frequently noted in the case of Bullfrogs
that certain places along the lake shore are occupied on successive
nights during the breeding season by single calling males, while

THE WAYS OF AMPHIBIA

405

no frogs are in the same place during the day. McAtee (1921)
reports a Bullfrog, readily distinguishable by a missing front foot,
being twice removed for considerable distances from its home
territory to new quarters along the same pond and each time
returning to the home site.

Although salamanders are able to learn a maze, they show little
homing instinct as far as is known. Storer (1925) found that
both Batrachoseps and Ensatina moved about considerably and
were not to be found on successive nights in the same retreat.

The most interesting cases of homing have been recorded among
frogs of a species that was comparatively slow in learning a
laboratory maze. Breder, Breder, and Redmond (1927) found
by carefully labeling individual Pond Frogs, Rana clamitans, that
two out of three caught in a spring and released several hundred
feet away on the other side of a stream returned to their home
spring, even though they had to cross the water where other Pond
Frogs resided. Moreover, an individual captured in the stream
and released in the spring returned to its home stream. Another
individual transferred from one pool near a stream to another
pool on the same side of the stream returned to its home pool,
even though other pools intervened and Pond Frogs were living in
both pools and stream. Further, there were no obvious differ-
ences in the character of the selected habitats. Hence, Pond
Frogs even out of the breeding season may have favorite terri-
tories to which they return. This is the more surprising in that
the species was found to be capable of a considerable random
wandering in the same locality.

Yerkes (1903) experimented with this same species of frog in a
maze which was arranged with the walls of one alley red and the
other white. After the maze had been learned, the color was
reversed. This change confused the frogs and they selected the
blind alley instead of the outlet, although their previous records
had been perfect. This shows that sight as well as kinaesthetic
stimulations entered into the learning process. Yerkes further
showed that Rana clamitans could remember a maze very well.
After a 30-day interval, there were 40 per cent of the mistakes at
the exit and only 20 per cent at the entrance. This was probably
explicable by the fact that the colors acted as aids at the entrance,
whereas at the exit there were no such important associational
clues. On the day after this series of trials, the record was
perfect. These data when combined with the field observations

406

THE BIOLOGY OF THE AMPHIBIA

reported above permit us to conclude that frogs are familiar with
details in their local habitats and that if they stray from this home
they may find their way back even after long periods of time by
making use of land marks to a large extent.

Voice. — The Amphibia were apparently the first vertebrates
to develop a voice. At least, some Carboniferous forms were
provided with a well-developed otic notch across which a tym-
panum was probably stretched. It is possible that the Rachi-
tomi used their ears only in detecting danger, but in the modern
frogs and toads with large tympana the voice is already well
established and used for a variety of purposes.

The chief function of the voice of frogs and toads is to attract
mates. Only the males are usually provided with a loud voice,
the females being either mute or only able to make cries lower
than those of the male. From detailed observations on tree frogs
it has been determined that the males select the breeding spot and
attract the females until they actually come in contact with the
body of the male singers. The males of other species, such as
Bufo and Scaphiopus, usually do not wait until the females
approach so closely but break off their singing abruptly and make
an effort to grasp any approaching individuals of either sex. In
the case of the American Toad it has been shown that the voice
of the male has a strong influence of attraction on the female
(Wellman, 1917). On the other hand, the South African Bufo
rosei is reported to lack a voice. How the males of this species
find their mates is not known.

Frogs and toads may be directed to ponds because of their
special sensitivity toward marsh odors or gradients of humidity
during the breeding season, but once they have arrived on the
breeding grounds the voice of the male would seem to play an
important role in restricting the range of the colony. Gold-
smith (1926) placed a series of Scaphiopus hammondii in an open
container and gradually approached a chorus of the same species.
At a distance of a mile the toads remained quiet, but when within
600 yards of the pool they became markedly active. At this
distance the chorus was very audible. There is no evidence that
toads hear better than man, and yet, since many species travel
long distances to the breeding pools, factors other than voice
must be of significance in these migrations.

Species which breed in temporary pools, such a the Spring
Peeper, Hyla crucifer, or the Spade-foot Toad, Scaphiopus hoi-

THE WAYS OF AMPHIBIA

407

brookii, often have louder voices than forms which spend their
lives near permanent bodies of water. Small species usually
have shriller voices than large species. Each species has its own
characteristic voice, and one of the surest ways of distinguishing
closely related species is to discriminate first between their voices
at night and then run them down separately with the aid of a
hand lamp. Often the voice of a grog or toad will give a clue
as to the relationships of a species. The southern toad, Bufo
terrestris, has nearly the same cry as the northern Bufo ameri-
canus, but the pitch is higher. Similarly, the southern Rana
sphenocephala has a higher pitched and more rapid call than the
northern Rana pipiens, although the syllables in the two cries
are very much alike. The two Cricket Frogs have a marked
similarity in voice. Acris gryllus crepitans, however, chirps
slowly two, three, or four times, and never are the syllables given
in the quick succession or the continuous rhythmic clicking which
characterizes the more northern Acris g. gryllus. The Swamp
Tree Frogs, Pseudacris, have recently been referred to Hyla, and
the voice of the species confirms this arrangement. Nigrita
has a voice almost exactly like triseriata, but the former barely
begins the crescendo of notes so characteristic of the latter. In
striking contrast, ocularis, which is structurally more Hyla-like
than the other species and climbs bushes in Hyla fashion, cries
in a shrill voice, "Pe-teet." Ocularis is apparently the smallest
frog in the United States and the cry " Petit" seems highly
appropriate. Of especial interest is the first syllable, which
has very much the quality of the familiar peep of Hyla crucifer.
Voice has also been used as evidence of relationship in some exotic
frogs, perhaps most recently by Blanchard (1929), in discussing
the relationships of certain species of Crinia in Tasmania. Where
related species are about the same size, the voices may be nearly
similar. Where size has changed frequently in evolution, it
would be dangerous to use voice characters as a clue to relation-
ships. In the chapter dealing with life histories, the hylas of
Santo Domingo have been considered a closely related group of
species, but they differ greatly in size and their voices have very
little resemblance.

When a frog calls, the mouth and nostrils are kept tightly closed
and the air is driven back and forth between lungs and mouth.
Usually one or two slits are present on the floor of the mouth, and
the air escaping through them is caught in a pocket of the sub-

408

THE BIOLOGY OF THE AMPHIBIA

hyoid or adjacent muscles which it dilates into one or more bal-
loon-like resonating organs. The sacs are diverticula of the
mouth-cavity lining covered by more or less thinned sheets of
muscle and skin. When the skin is so modified that it balloons
out into a large translucent sac under the chin or into a pair of
such sacs one on either side of the throat, the sacs are said to be
"external." But if the skin of the throat is not thinned, the
whole throat merely assuming a swollen appearance when the
frog calls, the sacs are said to be "internal." Closely related
species of a single genus, such as Hyla, may have different types
of vocal sacs, or again one distinctive type may be found in many
species of a genus, for example in the African Hyperolius. It is
remarkable that precisely the same type of vocal sac has evolved
independently in some of the Ranidae, Hylidae, and Bufonidae.

Bullfrogs and other species having internal sacs frequently call
under water. The voice of those species which have the external
type is modified if the sacs upon inflating meet some obstruction.
The Gray Tree Toad, Hyla versicolor, has two different calls : one
a melodious trill given with fully inflated pouch and the other a
feeble bleat, not unlike the cry of a young turkey, made when the
poueh is only half inflated. The western Hyla regilla and
apparently a few other tree frogs have more than one sex call,
but the males of the vast majority of Salientia have only a single
cry in each species. These cries range from the melodious drone
of the American Toad to the metallic clang of the Marsupial
Frog, Gastrotheca monticola; and from the clattering hammer of
the Carpenter Frog, Rana virgatipes, to the birdlike notes of
Hyla phaeocrypta. A few West Indian tree frogs (Eleuthero-
dactylus) may prove to have no voice at all, for they have never
been heard to sing, although extensively collected. Recent field
and laboratory observation indicates that Ascaphus is voiceless
even at the height of the breeding season. The frog lives in
rapidly flowing mountain streams, where the males would have
difficulty in making themselves heard.

Significance of Voice. — Besides the breeding call of the males,
most Salientia are able to produce a few guttural croaks or chirps.
As pointed out below, these sounds are of great importance to
frogs and toads in the recognition of sex. The females of several
European Salientia and one of our western toads, Scaphiopus
hammondii, have been credited with low voices (Storer, 1925).
Dahne (1914) described the voice of the female Midwife Toad,

THE WAYS OF AMPHIBIA

409

Alytes obstetricans, as louder than that of the male. Lankes
(1928) has recorded a voice in the female Hyla caerulea, feebler
but of higher tone than the males. It would seem that a distinc-
tive voice might aid in the recognition of sex, although no observa-
tions have confirmed this opinion.

Frogs and toads when escaping from their enemies will often
croak or chirp. The croak which usually accompanies the splash
of a frog into the water is, of course, well known. Many Salientia
when pinched or startled give vent to a very different cry. It
may be a scream, as in many ranas; a loud clatter, as in Scaphi-
opus holbrookii; or a shrill squeal, as in Eleutherodactylus inoptatus.
In all cases the mouth is held widely open, and the lungs are
only partly deflated at each note. Dickerson (1906) records that
both sexes of Hyla arenicolor may give such cries, and Lankes
(1928) reports the male Hyla caerulea giving it without provoca-
tion. The cry is often given when a frog is seized by a snake, and
while it may fail to frighten off the serpent, it may at least warn
other frogs in the neighborhood.

It is, perhaps, dangerous to speak of the emotions of so passive
a creature as a frog. But it should be noted that the reactions of
an individual toward the sex cry and the pain cry are totally
different. Voice in the frogs and toads has advanced beyond
its probable original use as a means of attracting mates together.
Many Salientia, such as the proverbial tree toad, will call loudly
when the humidity is suddenly raised. Some pond frogs call
after the breeding season has passed. These cries, like the sum-
mer songs of birds, may not be an expression of sex desire, but
with the limited repertoire at a frog's disposal they may be
precisely like the sex call. In the fall, with the ripening of the
gonads, some northern and many southern frogs begin to call
persistently. There are several records of species, which nor-
mally breed in the spring, having laid in the fall. Hence the
summer cries of frogs may be in their final analysis merely a
premature awakening of the sex instincts. There must be,
nevertheless, various grades of desire. Krefft (1911) reports a
female N ectophrynoides tornieri quietly listening to the song of a
male, and on several occasions I have found female Cricket Frogs,
Acris gryllus, sitting in a circle with heads directed toward a
calling male.

In urodeles the voice plays no part in the breeding process, and
most species seem to be silent throughout life. The newts

410

THE BIOLOGY OF THE AMPHIBIA

sometimes give a faint squeak when coming up to the surface for
air or when roughly handled in the water. The lungless Aneides
lugubris is known to be able to make a squeaking noise. Geyer
(1927) has recorded several instances of salamanders, both
lunged and lungless species, giving sounds. The larger sala-
manders, Siren and Amphiuma, have been credited with whistling
sounds, and the giant Megalobatrachus with a shrill cry. In all
these cases the sound is probably accidental and associated with
the sudden emptying of the lungs or buccal cavity. At least it is
not known to have any significant effect on the behavior of the
creature's associates.

Recognition of Sex. — It is frequently difficult for the collector
to distinguish the sexes of Amphibia in the field. How do the
breeding males distinguish the females from their own sex?
Females come to the breeding grounds attracted in part by the
call of the male. In the case of tree toads stated above, the
female may even follow the voice until she strikes the male's
body. Most male frogs and toads seize any object of about their
own size moving near them; a tree toad, when touched by the
female, turns and embraces her. Nevertheless, no male frog
recognizes the female as a sexual object. If the object embraced
possesses certain qualities it is retained until the time of egg laying.
The first requirement in the Wood Frog, Rana sylvatica, is a wide
girth and resistance to compression. Male Wood Frogs injected
with water until they had the same firmness as a female with
eggs were seized and retained as long as females (Noble and
Farris, 1929). A second requirement in the Wood Frog, and
especially in the common toad, is silence. The male frog, when
embraced by another, croaks; the female remains silent. This
differential action has been claimed to be the sole basis of sex
recognition, since males were supposed to disdain an embraced
partner which croaked. Male toads do not croak but chirp
when seized. A colony of breeding toads make a continuous
chirping sound, reminding one of a flock of young chicks in great
distress. There can be little doubt but that the warning croak
or chirp is one of the factors in sex recognition in some frogs and
toads, although Hinsche (1926) failed to find evidence of it in
the European toad, Bufo vulgaris. There are, however, other
factors which are equally important. Certain European Salien-
tia are said to interchange calls during the breeding season. The
subject is in need of further investigation, especially as the females

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411

of all American species have been found to be silent on the breed-
ing grounds, although some at least are capable of emitting loud
croaks at other times (Koppanyi and Pearcy, 1924).

The factors permitting sex recognition in frogs and toads would
seem to vary with the species, but in all cases there would seem to
be more than one. In addition to body size and silence there is
clearly an agitation factor in some forms. Hinsche obtained
evidence that it was the vibration of the flanks of the female
Bufo vulgaris and the jolting movements of her locomotion which
were chiefly responsible for the male retaining his grip. The
skin of the female B. vulgaris is rougher than that of the male,
and Hinsche found that smooth, hard objects induce failure of
the clasping reflex. Males would also not be held by the males,
because during the breeding season they change their gait
to a hop which makes that sex difficult to catch. There are
thus various factors both before and after the embrace which
insure that females will be seized instead of males and that they
will be held until the time of fertilization. In Rana esculenta,
Lullies (1926) found that the normal breathing movements of the
female during respiration stimulated the clasping reflex. At the
height of the season the reflex may be easily evoked in most
Salientia but the grip is retained only when other adequate
stimuli are present. In species which breed in colonies, the sex
calls of the males induce other males to call and the general chorus
and activity of the colony stimulates all participants. This in
turn seems to increase the speed and strength of the clasping reflex
but in the Wood Frog, at least, it does not produce a continuance
of the embrace unless the size and resistance requirements are
met. Male Wood Frogs release females after egg laying for the
same reason that they reject males at the beginning of the period,
namely, the body seized does not have sufficient girth or firmness.

The clasping reflex is, therefore, a means to sex recognition in
frogs. The spontaneity of this reflex rises and falls with the
season. During the breeding period a slight touch on the chest of
the male frog induces a vigorous clutching movement but out of
the season, no response. Busquet (1910) has shown that the
reflex may be evoked at other times of the year by cutting below
the medulla. The higher centers and, according to Busquet, the
cerebellum in particular exert an inhibitory influence on the
clasping reflex which prevents its functioning. During the breed-
ing season the testicular honmone counteracts this inhibitory

412

THE BIOLOGY OF THE AMPHIBIA

influence of the higher centers, permitting the clasping reflex
to come again into evidence. Hinsche has found evidence that
in some cases during the feeding activity of toads the embrace
reaction may be released, even though the toads were not at the
height of the breeding season. The mechanism by which the
higher centers were shunted off in this case is not known. It was
shown long ago that frogs raised in the dark have a greater reflex
excitability than those raised in the light (Langendorff, 1877) and
apparently because, as in the case of the clasping reflex, a domi-
nating higher center, vision, was prevented from functioning.

In urodeles the method of sex recognition seems to approach
that of mammals, for in the newt and all plethodontids secretions
are released from distinctive skin glands which play an important
role in courtship. In brightly colored European newts it would
seem that the difference of color between the sexes might have
some significance. In birds sight and sound alone apparently
suffice in discriminating male from female, but here the actions
of the two sexes are often very unlike. Various salamanders
engage in courtship antics, and their differential behavior finally
leads to breeding. In some fishes and Crustacea it is the different
behavior of the sexes when two breeding individuals chance to
meet which results in reactions leading to a fertilization of the
eggs (Holmes, 1916). In Amphibia the matter of meeting is not
left so much to chance. Frogs, with a few possible exceptions,
are endowed with voices with which they make their whereabouts
known, while salamanders frequently exhibit courtship displays
which tend to hold the sexes together. The salamanders, as
discussed in the previous chapter, have devised several ways of
making sure that the female will be present and in the proper
position for picking up the spermatophore when it is produced.
The olfactory sense seems to play the most important part in sex
discrimination in salamanders (Chap. XVI). Jordan (1893)
found that newts, however, would emit spermatophores when
only males were present. There are several factors involved in
the courtship display of newts and other salamanders.

Parental Instinct. — Few other instincts have contributed as
much to the success of higher vertebrates as that of parental
care. This first manifested itself among vertebrates in a brooding
instinct or tendency for one or more parents to remain with the
eggs. The instinct appears in a very complex form among

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413

various invertebrates and fish; among Amphibia it seems to have
independently developed several times.

In the hynobiid salamanders the males remain with the eggs
for varying periods to fertilize them. They exhibit an active
interest in the eggs and drive the females away in their struggle
to gain possession of the eggs. As stated above, the crypto-
branchids which have evolved from hynobiids extend this guard-
ing until the eggs hatch. Both sexes devour the eggs, but as
the guarding male can eat only a small proportion of them,
this habit has not interfered with the success of the species. Most
Amphibia which lay their eggs in the water abandon them after
fertilization, but among those which deposit large-yolked eggs,
the female frequently remains with them. Whitman (1899)
conceived that the chief utility of this brooding instinct was
originally the rest it gave to the parent following oviposition.
The protection afforded would be quite sufficient to insure the
development of the instinct, natural selection favoring those
individuals which keep their position long enough for the eggs to
hatch.

The brooding habit is well established in the primitive pletho-
dontids. Since many of these forms, such as Gyrinophilus
danielsi, lay their eggs under stones in streams, the protective
value of the instinct is not very great. The habit, however,
was carried over to the specialized terrestrial plethodontids where
this aspect becomes of the greatest importance. The damp body
of the parent assures the eggs sufficient moisture, and her dermal
secretions apparently prevent mold from growing over them;
at least eggs of some species removed from the parent are usually
destroyed by mold. The habit has permitted some forms such
as Aneides lugubris to lay their eggs in comparatively dry
situations.

The bond between parent and eggs is so strong that some terres-
trial plethodontids will move their eggs with them when dis-
turbed, and most return to the egg mass after being frightened
away (Fig. 136). This return of the mother to her charge has
been witnessed also in the large Amphiuma which, although
primarily an aquatic form, lays its eggs under logs on land. The
nature of the sensory impressions directing the parent, whether
olfactory, optic, or something more subtle, is entirely unknown.
Wilder found that a female Desmognathus fuscus will brood the
eggs of another female if these are suitably arranged. Hence a

414

THE BIOLOGY OF THE AMPHIBIA

female salamander apparently does not recognize its own eggs.
The bond between parent and eggs may be considered an instinct
and as such to have arisen in the same way as other instincts
(Chap. XVI).

The brooding instinct seems to have arisen fully formed in
many groups. Thus, most species of Ambystoma abandon their
eggs in the water, but A. opacum deposits its eggs on land in the
fall and curls around them. Although the terrestrial eggs of
Desmognathus and other salamanders are sometimes found with-
out parents, it seems probable that the parents may have been
destroyed, rather than have failed to exhibit the brooding instinct.
It has been shown that A. opacum, however, does not return to
its eggs when disturbed. Hence, the bond between parents and
eggs is not great in this species, and the brooding habit may have

Fig. 136. — Female Desmognathus fuscus brooding her eggs.

resulted merely from exhaustion of the female after egg laying.
The brooding of Necturus may have even less biological signifi-
cance. Bishop (1927) found that females occupy the "nest"
after the young have departed. Since some adults use these
nests as retreats throughout the year, the brooding of Necturus
may be merely the result of the disinclination of the adult to
leave a favorite retreat.

In higher vertebrates an extension of the brooding instinct leads
to care of the young. Among salamanders only some terrestrial
plethodontids, Aneides (Storer, 1925), Hemidactylium (Blan-
chard, 1923), and possibly Plethodon remain with the young after
they hatch. In these cases probably little or no protection is
given to the young, unless it be that the moist body of the parent
prevents their desiccation. Among frogs the habit of brooding
the eggs has led to various modifications of the female's body.
Protopipa and Pipa carry the eggs in individual sacs on the back

THE WAYS OF AMPHIBIA

415

until the young hatch fully formed. The Marsupial Frogs,
Gastrotheca, employ a single sac, and the young may escape as
tadpoles or as metamorphosed frogs. In the case of Gastrotheca,
the origin of the sac may be traced to shallow folds border-
ing the egg mass carried on the back of the female Cryptobatra-
chus. Once the brooding habit was established in this group of
South American tree frogs, it led to marked structural changes in
the parent. Less marked changes of the integument have been
noted in other brooding frogs, but in no case have emotional
bonds been established which make possible the protection of the
young after hatching.

The males of various species of frogs have been found guarding
the eggs. This habit may not be a true brooding instinct but
merely the tendency of the males to remain near their calling
stations. In some forms, however, such as the Australian foam
nest builder, Adelotus brevis, there seems to be a real attraction
of the male parent (Deckert, 1929) toward the eggs. This habit
seems to have led in the neotropical Phyllobates and Dendrobates
to the male's transporting the tadpoles apparently from the place
of egg laying to the pools (Noble, 1927). It also may have led
to the remarkable habit of the male Rhinoderma of carrying its
eggs in the vocal pouch until the young are fully formed.

Feeding Habits. — Frogs and toads eat animal food when adult
and either animal food or plant food when larvae. The bulk of
the food consists of insects, spiders, millipeds, snails, worms, and
similar small fry. It was found in the laboratory that toads
could learn after a single experience to avoid an obnoxious insect,
and Haber (1926) has observed a toad attempting to disgorge a
stinkbug (pentatomid), which it had seized. Insects giving off
acrid or irritating substances were found by Haber to form but a
small portion of the diet of Hyla cinerea. Nevertheless, it has
frequently been noted that neither frogs nor toads have marked
food preferences. Goldsmith (1925) found that the Spade-foot
Toad, Scaphiopus hammondii, devoured all types of surface
insects, ants of the genus Atta being the predominant form. The
diet varies more or less with the habitat of the species; frogs
naturally capture more aquatic forms than toads do. Detailed
studies have been made of the diet of frogs (Surface, 1913; Drake,
1914; Munz, 1920), tree frogs (Storer, 1925; Haber, 1926), and
particularly the common toads (Kirkland, 1897, 1904; Hodge,
1898; Garman, 1901; Kellogg, 1922), while some observations are

416 THE BIOLOGY OF THE AMPHIBIA

available on species of other genera and families (Noble, 1924).
Ants and termites, which are eaten by most Salientia, rise to a
high percentage in certain slow-moving, burrowing types, while
they almost disappear from the diet of aquatic forms. Many
large and a few medium-sized frogs have been found to be canni-
balistic. This is particularly true of the larger species of Cera-
tophrys of South America and the brilliant Rana ornatissima of
Africa, but observations are not sufficiently numerous to deter-
mine what percentage of their yearly diet consists of their fellow
frogs.

It is interesting that the tadpole of Ceratophrys ornata should
be largely cannibalistic, feeding on the larvae of other frogs.
Tadpoles in general show greater food preferences than adult
frogs, for some are exclusively vegetarian, others carnivorous,
while the majority take a mixed diet. The common water silk,
Spirogyra, forms one of the best foods for most tadpoles reared in
the laboratory. This diet may be varied with strips of water-
soaked beef which foul the water less quickly than pieces of
earthworm.

Terrestrial Salientia, and especially toads, although indis-
criminate feeders, are of economic value, for they devour the
dominant insects or other invertebrates of any one locality; and
around greenhouses, gardens, or farms such dominant forms are
usually pests. Kirkland (1897) found that enough food was
taken by the common toad to fill the stomach completely four
times in 24 hours. Pack (1922) records a case where the toad was
of real value in fighting an outbreak of sugar-beet webworms.
If toads could be transported in great numbers across the coun-
try, they might be of service in counteracting plagues.

Urodeles apparently restrict themselves to an animal diet
during both larval and adult life. They show a greater tendency
to take quiescent food than most frogs. Thus Necturus has been
reported to devour great numbers of fish eggs and Cryptobran-
chus, Pleurodeles, Salamandrina, Ensatina, and Aneides have on
occasions eaten their own eggs. Storer (1925) is inclined to
believe that fungus found in the stomach of the latter form was
eaten intentionally. Similarly, algae taken from the stomach
of Siren has been described as present in too great a quantity
to have been devoured accidentally with the animal food known
to form a large part of their diet (Dunn, 1924). Size may have
an important influence on diet. The small Salamandrina does

THE WAYS OF AMPHIBIA

417

not feed well on Enchytraei, apparently because the small tongue
is fitted only for the capture of dry food such as insects (Klingel-
hoffer, 1930). As in the case of frogs, the larger species are fre-
quently cannibalistic. Dicamptodon, Ambystoma, Gyrinophilus,
and Aneides have been reported to eat smaller species of sala-
manders. In the laboratory the large Desmognathus quadra-
maculatus may be kept in good health on a diet consisting of
smaller species of Desmognathus exclusively. No species of
urodele is known to restrict its diet to a particular kind of animal
food.

The different manner of capturing prey would account for
such differences as exist between the diet of adult frogs and
urodeles. Hargitt (1912) found that tree frogs usually leap
to take their prey, rarely stalking it. They usually wait for the
prey to come within leaping distance, which may be a matter of
several feet, and when they spring they rarely miss. If the prey
should come within close range, it is apparently not seen. In
striking contrast the response of newts to a moving object is a
stealthy approach. The object is then nosed and if found satis-
factory the snapping reflexes are evoked (Copeland 1913).
Newts will snap at movable inedible objects and also at invisible
edible substances such as fine suspensions of beef juice. Some
newts will feed after their optic and olfactory nerves are cut and
when the lateral-line organs alone are apparently functioning as
distance perceptors (Matthes, 1924) . Hence, while the normal
order of events in the feeding process is optic stimulations induc-
ing the approach reaction, followed by olfactory stimulations
evoking the nosing and finally the snapping reactions, the last
reaction may be called forth by sight, smell, or lateral-line
stimulation alone.

Smell has also been found to function without vision in the case
of Ambystoma larvae (Nicholas, 1922). Smell would seem to be
of great importance to Amphiuma, for Hargitt (1892) found that
clams form a large part of its diet. Whether aquatic Salientia
depend more on smell than terrestrial ones do is not known, but
the evidence suggests that vision may be used to the exclusion of
smell in some land forms. Such species would not be able to
devour eggs or other immobile food, for it is a moving object in the
field of vision which excites motor reactions in most Amphibia.

The evolution of the higher groups of vertebrates seems closely
correlated with changes in food habits. There is little evidence

418

THE BIOLOGY OF THE AMPHIBIA

of such correlation in Amphibia. Gyrinophilus, perhaps the
most cannibalistic plethodontid, does not have proportionately-
longer teeth than many small species of the same family. The
marked changes of dentition within such genera as Desmognathus
is not known to have any correlated changes in diet. Morpholog-
ical change may have induced a few restrictions of diet. The
large toads of Africa feed rarely if ever on mammals, whether
or not this is due to their toothless jaws (Noble, 1924). The
narrowing of the mouth in the Pipidae may have brought certain
adaptive changes especially in the fingers which became impor-
tant aids in feeding. No other Amphibia stuff their food into
the mouth with their fingers nor even habitually hold the food
with their forelimbs while devouring it. But the tongueless
Xenopus is very adept in seizing its prey with its long fingers
and forcing it into its comparatively small mouth. In Pipa a
rosette of papillae tip the ends of each finger and are provided
with tactile organs which apparently aid in locating living food.

Long teeth when they occur in the Amphibia are frequently
used to good effect. Powerful jaws have no doubt been of
assistance to the tadpole of Ceratophrys ornata in devouring other
tadpoles. The adult of this species has enlarged dagger teeth
in the upper jaw which are said to serve as effective weapons.
Dr. W. M. Mann found that the Solomon Island Ceratobatra-
chus, which unlike most frogs has teeth in both jaws, exhibited
bulldog tenacity in holding to a seized object.

Responses to Temperature Change. — A lowering of tempera-
ture below 8°C. was found to induce laboratory frogs to seek a
retreat under objects in the bottom of the tank (Torelle, 1903).
As pointed out by Holmes (1927), this may not be so much a
reversal of the phototropism as a release of instincts to dive down
and crawl under objects. The normal stereotropic response of
toads is more pronounced at low than at high temperatures
(Riley, 1913). Toads burrow into the ground on the approach
of cold weather and while digging with their hind feet
presumably keep their original orientation as regards fight.
Toads may burrow to a depth of 18 inches in sandy soil and 8
inches in clay ground (Butler, 1885). Frogs hibernate in mud
in the bottom of ponds, in springs, or in damp spots in the woods.
Some merely dig under decaying vegetation or other debris in
their normal habitats. A single species may hibernate in differ-
ent situations in different parts of its range. McAtee found that

THE WAYS OF AMPHIBIA

419

Eurycea bislineata in Indiana will come out of the water in
November and pass the winter under logs and stones near
streams. In the New York region the same species is never
found on land in midwinter but may be collected in numbers by
turning over the stones in the deeper portions of flowing streams.

Brooks (1918) found that between the temperatures of 5 and
20°C. the warmer the water the greater the time Rana pipiens
spent at the surface. No doubt other frogs would be affected
the same way, although each species would have its own range of
response. Cole (1922) found that the higher the temperature
the shorter the reaction time to light. Lutz (1918) showed that
warming lowers the thresholds for both reflex and nerve-muscle
responses in the frog. Between 4 and 30°C. the reflex threshold
is lowered to a much greater degree than the nerve-muscle thres-
hold. Hence temperature would seem to act directly on the
synapse between the neurons in the reflex arcs. At low tem-
perature the normal reflexes to environmental stimulations are
unable to appear. It may be noted also that the integumental
sense organs of the frog require a higher temperature to induce a
response if the temperature increase is gradual than they do if it is
sudden (Morgan, 1922), and, hence, sudden changes in tempera-
ture would have a more marked effect on frogs in nature than
gradual ones.

Wright (1914) finds that most species hibernating on land are
responsive to climatic changes earlier than those hibernating in
the water. The rule does not always hold, however, for hiber-
nating H. crucifer, an early breeder, has been found in springs
in midwinter, while H. versicolor, a late breeder, digs down in the
debris in the bottom of the holes in the trees where it spends the
late summer. Brook salamanders such as Desmognathus fuscus
hibernate under rocks in running water, and here it cannot be
merely a negative phototropism which brings them there. Pond
species, such as the newt, usually remain in the ponds during the
winter, although from the observations of Wolterstorff (1922) cold
must slow down their activity greatly. Szymanski (1914)
recorded on a kymograph the movements of Salamandra during
hibernation. From November to January there was no move-
ment of the body, although a slight change occurred in the posi-
tion of the limbs. Tiger salamanders have been described as
passing the winter in the bottom of the pools (Shelf ord, 1913).
Other species of Ambystoma, such as A. maculatum, undoubtedly

420

THE BIOLOGY OF THE AMPHIBIA

hibernate on land. In spite of the different temperatures of these
situations the two forms breed almost simultaneously in the East,
the water-hibernating species a little before the land-wintering
form.

Since egg laying is controlled by the secretions of the anterior
pituitary gland, the functioning of the latter is apparently
influenced by temperature. Barthelemy (1926) records Rana
fusca, however, exhibiting an increase in weight, i.e., evidence
of sexual activity, in the spring even when low temperatures were
maintained. Hence, hormone control is partly free from temper-
ature control.

The utility of hibernation is obvious. Levy (1900) found that
frogs could live under water at temperatures of from 0 to 9°C.
without injury for long periods, while they would surely die if
they attempted to winter in their usual habitats. Some Euro-
pean frogs have been credited with surviving temperatures of
— 4 to — 6°C. (Muller-Erzbach, 1891). Rana pipiens dies at
temperatures a little lower than a degree below freezing. Cam-
eron (1914) found that death was due to a specific temperature
effect on the coordinating centers of the central nervous system.
The heart tissue survives at temperatures nearly 3° below freezing
and the body-muscle tissue at practically the same (Cameron
and Brownlee, 1913). Frogs and salamanders frozen in blocks
of ice frequently survive for short periods. In the case of
Amphibia hibernating on land, the dryness of the winter air would
have a detrimental influence perhaps equal to that of the cold
(Hecht, 1928).

Frogs frequently mate in the spring directly after coming from
hibernation. Barthelemy (1926) found that hibernation was
necessary for the maturation of the eggs of Rana fusca. Hiberna-
tion was found not to be essential, however, for the health of
various Californian toads, frogs, and tree frogs. Rana aurora
draytonii, for example, hibernates in some California localities but
not in others. Frogs in the laboratory do not hibernate unless the
temperature is lowered.

Temperature Preferences. — Amphibia frequently change their
habitat at the time of hibernating. Abbott (1882) describes the
Cricket Frog, Acris gryllus, as leaving the ponds and migrating
to rocky ravines in the fall where it hibernates under stones and
logs out of water. Terrestrial salamanders, such as Desmognathus
fuscus carolinensis, hibernate under rocks in mountain streams.

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421

Where many salamanders have been found together in
hibernating dens, as, for example, in the case of Salamandra
salamandra, there must have been some movement in the fall if
only to look for suitable hibernating quarters. Such movements
never take on the appearance of the spring migration, but they
have various parallels in the fall migration of some birds and
mammals.

The various species of Amphibia have certain temperature
optima at which they live best. This may be only a few degrees
above freezing in the case of Ascaphus, which lives at high alti-
tudes in northwestern United States. Frog tadpoles frequently
seek the warmer margins of pools whether they be attracted
there by the greater light or by the higher temperature. Brues
(1927) found the tadpoles of various frogs in the hot spring
waters, ranging from 104 to 106°F. Most Amphibia cannot stand
high temperatures for any period, the optimum for both Rana
pipiens and Necturus lying near 18°C. (Sayle, 1916; Cameron,
1921). The greater temperature tolerance of Eurycea multi-
plicata over that of Typhlotriton is apparently the chief factor
permitting the former to wander in and out of caves. Reese
(1906) found that Necturus was affected more than Crypto-
branchus by extremely high temperatures, however, and yet the
former lives in a greater variety of habitats. Hence, in one
species, temperature may have an important control over dis-
tribution and in another, other factors may be more important.
It may be said that attempts to determine the ability of Amphibia
to* discriminate between temperatures have not been successful.
Pearse (1909) found that toads in the dark were indifferent to a
steam pipe and salamanders in the laboratory usually react
poorly to gradients of temperature.

Responses to Humidity Change. — Amphibia with their thin,
moist skins are very sensitive to changes in humidity, and their
habitat selection as well as their daily movements may be con-
trolled to a large extent by their reaction to this change. Gold-
smith (1926) found that digging reactions were induced in the
Spade-foot Toad, Scaphiopus hammondii, by evaporation, and
this species was sensitive to a humidity change of 10 per cent at a
temperature of 27°C. Shelford (1914) studied the effects of
evaporation on both frogs and salamanders. Responses occurred
whether the evaporation was due to the dryness, warmth, or
movements of the air. Plethodon glutinosus was clearly more

422

THE BIOLOGY OF THE AMPHIBIA

sensitive than the much smaller Plethodon cinereus. This is
surprising, for the surface per unit of weight is greater in small
objects. The observation is of especial interest, for it gives an
explanation as to why the former species lives in damper situations
than the latter. Both salamanders and frogs were stimulated at
once by dry air and endeavored to avoid it. Toads survived
the treatment longer than frogs, a fact which would be expected
because of their thicker skins. Shelford suggests that the
responses of Amphibia to humidity change may be due to a
disturbance in the neutrality of the body fluids due to the
changing rates of evaporation. Probably the drying of the skin
would also have a direct effect on the integument al sense organs.
Rapid drying is far more serious to the health of Amphibia than
slow drying. Frogs die after a loss of less than 15 per cent of
their weight if the evaporation is rapid, while they may survive
nearly twice this loss if it is slow (Kunde, 1857). Toads may
even stand a loss of 50 per cent of their weight (Langlois and
Pellegrin, 1902), a great increase in the density of their blood
occurring during the experiment.

Most Amphibia wander at night when the humidity is greater
than during the day. The migrations and breeding of many
frogs and salamanders are initiated by the rains, although the
temperature factor may also be important as well. Many small
tree frogs have the same climbing mechanisms of large species
but they rarely ascend tall trees, apparently because of the
high evaporation rate of such an exposed position. At times of
draught the amphibian inhabitants of certain ponds or trees may
come together in the damper or more favorable shelters. Var-
ious species of desert frogs have been described as undergoing
a true aestivation. The Sardinian cave salamander, Hydromantes
genet, has been reported to aestivate during the summer months
even in the laboratory where moist conditions were presumably
maintained (Mertens, 1923). Whether or not any of these
Amphibia really aestivate, there is no doubt that the different
humidity requirements of the various species are one of the most
important factors limiting their ranges and activities.

Defense. — Amphibia have few methods of defending them-
selves from their enemies. As a group they are relatively immo-
bile. Their habit of maintaining a fixed posture between
movements results in their frequently being overlooked by
possible enemies. Their first reaction to distant disturbances is

THE WAYS OF AMPHIBIA

423

an inhibition of all movement, even the respiratory movements
of the throat. When danger approaches, they usually seek
safety in flight, most seeking crevices and other natural shelters,
a few, burrows which they had previously dug. Some of the
larger species apparently defend themselves by biting. This
is true of Gyrinophilus, Cryptobranchus, Aneides, as well as the
usually good-natured Plethodon glutinosus and Desmognathus
fuscus. Diller (1907) found an 8-inch Ambystoma with a grip on
a 2-foot garter snake, and it was apparent that the salamander
was having the better of the struggle. The large South American
frog, Ceratophrys dorsata, can inflict a serious bite and does not
hesitate to use its teeth when annoyed. In this species, as in
various forms of Rana, the mento-Meckelian bones originally
used for closing the nostrils are hypertrophied into a formidable
spike. Brook salamanders, such as Desmognathus and Eurycea,
are able to twist strenuously in the hand when seized, and Amphi-
uma is notorious for its ability both to bite and to twist at the
same time.

Frogs in the act of leaping often release the contents of their
urinary bladders, thus lightening their bodies and screening their
path of retreat. Amphibia receive their chief protection from
their skin glands, the mucus making them slippery and difficult
to hold, while the poison or granular glands have frequently a
serious effect on such tissues as the lining of a dog's mouth.
Some burrowing Salientia, especially certain Spade-foot Toads,
develop secondary deposits of bone in the skin of the head.
In a few genera (Ceratophrys, Melgalophrys, and Brachycephalus)
of unrelated families, this deposition of bone may extend to
the skin of the back. A number of tree frogs, Hyla, Gastrotheca,
etc., develop a similar armature, and the correlation of secondary
bone deposits and special habitats is not close.

Certain movements of Amphibia may increase the flow of the
skin secretions. The "warning attitude" of Bombina is accom-
panied by such a flow. The salamander, Ensatina eschscholtzii
(Fig. 137), stands high on its legs when annoyed and waves its
tail, which actively secretes (Hubbard, 1903). Frogs and toads
have a limited repertoire of defense reactions. Most species will
blow up their lungs, close the eyes, and bend the head in a crouch-
ing attitude. Hinsche (1923) finds that this reaction is called
forth in toads by either tactile or visual stimulations but not by
sounds. It is better developed in old than young individuals.

424

THE BIOLOGY OF THE AMPHIBIA

Many frogs and toads when pinched will open their mouths
and give a shrill cry. It would seem to be an important frighten-
ing device, although critical field observations concerning its
effectiveness are lacking. Hinsche (1923) finds that this fright-
ening reaction may be induced in Bufo, but the toad opens its
mouth and straightens its legs without producing a sound.
Hinsche (1928) has shown that the head-bending and leg-
straightening reaction is part of a complex series of defense reac-
tions common to many Salientia. In the course of phylogeny,
some parts of this series of reflexes, such as the warning cry, are
lost, while other phases, such as the pushing with bowed head,
are modified. It is interesting that the more terrestrial Salientia
should exhibit the series of reflexes in their most developed form.
As discussed in another chapter (page 381), many reflexes, such
as the "unken reflex" and the scream reaction, exhibit a gradual

Fig. 137. — Ensatina eschscholtzii defending itself against a Ring-necked Snake.

{After Hubbard.)

modification in phylogeny but the change is not always closely
correlated with an obvious utility.

Tonic Immobility. — Salamanders, frogs, and toads may be
readily thrown into a state of tonic immobility which, under
certain circumstances, may prove a protective measure. Young
toads when picked up will frequently partially contract their
limbs and become immobile (Mangold, 1925). This behavior
has been compared with the hypnotic state produced in man by
suggestion. It is commonly seen in such salamanders as
Plethodon and Ambystoma, which when handled gently often
exhibit a "death feint." It may be most readily induced in
both frogs and salamanders by placing the individual on its back
and holding it there a moment. The death feint usually lasts
only a few minutes, but it may be prolonged over an hour if
disturbing sensory impressions are avoided. A sudden tactile
or visual stimulation will arouse the frog or salamander from this
state.

THE WAYS OF AMPHIBIA

425

Mangold and Eckstein (1919) have studied the reflex excit-
ability in certain European frogs which had been hypnotized, that
is, thrown into this state of tonic immobility. This was tested
by counting the number of electric shocks necessary to induce
the springing reflex when these stimulations were of the same
intensity and given at the rate of 21 to 24 per minute. They
found a decided lowering of the reflex excitability in hypnotized
frogs. The degree of lowering was dependent on the depth of
the hypnotic state. Frogs hypnotized by being placed on their
back were much less sensitive to stimulations than those hypno-
tized belly down. This is correlated with the more easy induce-
ment of hypnosis and slower awakening of frogs placed on their
back.

The protective value of tonic immobility in Amphibia is not
great. In certain birds brooding their eggs in exposed situations
and in certain insects which resemble twigs, the ability quickly
to assume and hold a stiff posture on the approach of danger has
great survival value. In these forms the stimulus which frightens
the creature sets up the hypnotic state. In Amphibia hypnosis
is produced only by sudden tactile stimulations, although a more
extended development of this type of response might have great
advantages.

Leaping of Salamanders and Frogs. — One of the most sur-
prising escape reactions of salamanders is the leaping movements
of terrestrial plethodontids. The tail is struck sharply against
the ground at the same moment that a spring is made with the
short legs. The combined effect is a leap frequently greater than
the length of the animal's body. In such a defenseless creature
as Plethodon cinereus this leap may well be an important method
of escape, but it may also be a means of aggression, especially
useful in capturing food.

The tails of many terrestrial salamanders when seized may be
readily thrown off by their owners. The mechanism of this
autotomy is different from that in lizards, the break occurring
in the myoseptum and extending between the vertebrae. In
lizards a special breakage plane is developed across each vertebra.
Autotomy in salamanders resembles that in lizards in that the
musculature is broken off nearer the tail base than the skin is.
The raw flesh on the freed tail induces writhing movements in
the discarded appendage, while the extra skin on the tail base
curls over the wound and facilitates healing. In a few terrestrial

426

THE BIOLOGY OF THE AMPHIBIA

plethodontids such as Hemidactylium and Ensatina a double or
single groove occurs around the tail base and the split occurs
here instead of anywhere along the tail as in Plethodon.

One mechanism of escape which has a strong appeal to the
imagination is found in the much discussed " Flying Frog" of
Borneo and adjacent regions. Wallace, in his " Malay Archi-
pelago," tells of the tree frog, Polypedates nigropalmatus, which
has large webs between all its digits, being brought to him by a
Chinese workman who claimed he had seen it engaged in a slanting
flight from a high tree. Recently Ayyanger (1915) has recorded
a slanting flight of 30 or 40 feet in the related Polypedates
malabaricus. Cott (1926) watched tree frogs of a different
family in Brazil and saw Hyla venulosa voluntarily leap off into
space at a height of 40 feet from the ground. In a series of
experiments Cott concluded that this species could fall 140
feet or more without injury. No doubt smaller frogs could fall
even greater distances without injury because of their relatively
greater surface as compared with their weight. Little frogs as a
rule do not climb tall trees, however.

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CHAPTER XVIII

THE RELATION OF AMPHIBIA TO THEIR ENVIRONMENT

Frequent reference has been made above to the close relation
between Amphibia and their environment. Certain aspects
of this subject require further consideration.

Metabolism of Amphibia. — Amphibia are cold-blooded; they
lack the mechanisms which give the higher types both freedom
from environmental change and constancy of chemical activity
at the optimum conditions for the expenditure of their energies.
Low body temperature means slow chemical changes, such as
those of digestion, also lower velocity of nerve conduction and a
throttling down of many other body activities which in the
homoiotherms produce a more active and efficient organism.
Thus the digestive enzymes of both salamanders and frogs exhibit
their greatest degree of activity at about 37°C, which is the
optimum temperature for mammals (Kenyon, 1925). Such a
body temperature is practically never realized in Amphibia.
In fact, most Amphibia are so adjusted they would die at that
temperature. Hence their energy sources, the food and oxygen,
are made available at a much slower rate in these forms. The
range of metabolic rate in Amphibia is from eighteen to one
hundred eighty times slower than that of small mammals and
birds. Amphibia are not able to make use, to the fullest extent,
of either their nervous or their motor systems. They remain
slaves of their surroundings.

Although in a general way Van't HofFs law that the velocity
of chemical process is approximately doubled for every rise of
10°C. applies to metabolic processes in amphibians and has been
shown by Laurens (1914) to hold for the rate of the heart beat in
Ambystoma, its applicability is not absolute. Krogh (1916) has
reviewed the works of investigators showing that the "law"
applies better in the intermediate ranges than at high and low
temperature extremes. Oxygen consumption has been found
greater at low temperature and lower at high temperature than
the amount expected by this law. Furthermore, the seasonal
maximum of metabolism does not necessarily come at the height

431

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THE BIOLOGY OF THE AMPHIBIA

of summer heat but rather appears during the mating season, in
early spring. This is undoubtedly due to the influence of internal
secretions set up by the sexual cycle and indicates the profound
regulatory and modifying effect of hormonic influences on chem-
ical processes, which otherwise would appear to conform strictly
to inorganic laws.

Many factors influence the body temperature and hence affect
the metabolism of Amphibia. Water is such a good conductor
that immersed Amphibia follow closely the temperature of their
aquatic environment. Water affords a very stable medium which
does not undergo the sudden fluctuations of temperature peculiar
to the land environment. The skin of Amphibia is moist and
the loss of heat on land through evaporation may be greater than
the actual heat production of the animal. Rubner (1924) found
that in Rana esculenta at 3°C. the cooling by evaporation would
lower the body temperature to only half a degree above freezing;
while at 30°C. the body temperature dropped to 25.4°C. In
dry air, frogs are always colder than their environment, while in
high humidities they are warmer than their surroundings (Isser-
lin, 1902). Tree frogs have on various occasions been reported
resting on leaves exposed to the direct rays of a scorching tropical
sun. In these cases the temperature of the frogs was probably
considerably below that of the surrounding atmosphere. The
moist skin affords the Amphibia a protection against overheating,
but as the skin itself is subject to rapid desiccation, few Amphibia,
other than the rough-skinned toads and salamanders, will remain
long in a dry atmosphere. These rough-skinned species depend
largely on their lungs to prevent overheating. The pulmonary
evaporation mechanism is extensively employed in higher verte-
brates for the lowering of body temperature. The loss of heat
through the skin or lungs of amphibians, is a temperature-
regulating mechanism in its primitive form. Since the mecha-
nism of keeping the skin moist is dependent on the environment,
it further restricts the habitat of these animals.

The pigmentation of an amphibian may affect its body tem-
perature considerably. Most species when cold expand their
melanophores. Arboreal species or forms living in exposed
situations and subject to the cooling effect of winds on their
moist skin are often able to change their coloration quickly.
This is usually considered a concealing device, but it may equally
function as a regulator of body temperature.

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 433

Temperature and Behavior. — Amphibia usually respond
adaptively to thermal change. Frogs retreat to hibernation on
the approach of cold weather and reappear on the advent of
spring warmth. Each species, however, has its own temperature
level to which it responds. Some salamanders, such as Gyrino-
philus porphyriticus, select colder waters in which to live, and
others, such as Necturus, undergo an annual migration to waters
of warmer temperature. Species differ i considerably in their
range of tolerance and this range may determine their distribution
or their time of appearance. Tropical frogs do not live well at
temperatures northern frogs enjoy. In the case of the Indian
Rana hexadactyla, Garten and Sulze (1913) showed that a cessa-
tion of reflex excitability occurred at 5°C, which is several
degrees above the critical temperature for northern frogs of the
same genus. Many forms, however, are able to acclimate them-
selves to a marked change of temperature if given a sufficient
time. Davenport and Castle (1895) found that the upper limit
in toad tadpoles could be increased several degrees, and these
tadpoles are occasionally found in nature in water which is
uncomfortably warm to touch. At the other extreme, Bufo lives
in the Himalayas at an altitude of over 14,000 ft. and Scutiger
has been collected 2,000 ft. higher in Tibet.

The relative humidity is well known to influence the movements
of Amphibia. Since the skin is moist, it acts very much like
the wick of a wet-bulb thermometer and depresses their body
temperature below that of the environment. Hall and Root
(1930) found that in an atmosphere of 7 per cent relative humidity
at 20°C. Plethodon glutinosus suffered a depression of 9.21°,
Rana pipiens 8.60°, and Bufo fowleri 7.33°. Thus the toad with
its relatively drier skin was influenced least by the dry air. By
way of contrast, certain rough-skinned lizards showed very little
lowering of body temperature at the same humidity. Lowering
of the body temperature is known to bring into function various
reflexes not exhibited at higher temperatures (Chap. XVI).
Hence humidity may have a far greater influence on the behavior
of moist-skin Amphibia than it does on reptiles with their dry
skin. Frogs may be warmer and better able to use their digestive
and nervous mechanism on a rainy day than on a dry, sunny day.
The development of a dry skin in the early reptiles was an impor-
tant step in the direction of homoiothermism which the Amphibia
failed to follow.

434

THE BIOLOGY OF THE AMPHIBIA

Metabolism and Behavior. — Specific differences of behavior
may be due in part to specific differences of metabolism. Helff
(1927) showed that marked differences in oxygen consumption
existed between several species of Ambystoma. It was interest-
ing to note that A. tigrinum, the most aquatic species, had the
lowest rate. This is in keeping with the observations of Cron-
heim (1927) : that the terrestrial Rana temporaria absorbed more
oxygen than certain aquatic European frogs. Amphibia during
metamorphosis undergo a rapid increase in oxygen consumption.
The immediate cause for the adoption of land life might be in
these cases a greater need for oxygen, but the oxygen need in
turn would be conditioned by the specific metabolic rate which
fluctuates around a certain mean.

Fuel of Metabolism. — Food is the fuel of metabolism. Starva-
tion of frogs may result in a 40 per cent decrease in metabolism
within a week (Hill, 1911). In these forms a low metabolic level
was reached during inanition in 15 days and no marked drop
occurred after this time. Hill suggests that the glycogen stores
may have been exhausted after a week, and a shift from carbohy-
drate to fat metabolism may have occurred. Fat oxidation gives
a lower energy supply than glycogen, hence is the chief source of
energy for Amphibia during hibernation. Amphibia, like many
mammals, tend to store fat during the summer and to utilize this
food source during winter hibernation (Athanasiu, 1899; Dolk
and Postma, 1927).

Small mammals are required to eat proportionately to their
weight a greater amount of food than large mammals in order to
keep warm, for their surface, which radiates heat, when compared
with their bulk, is proportionately greater. Rubner (1924) has
presented data which suggest that the " surface law" of decreas-
ing energy consumption in relation to decreasing surface is appli-
cable to amphibians when only a single species is considered.

Hormones and Metabolism. — The metabolism of Amphibia is
greatly affected by the secretions from the glands of internal
secretion, especially by the thyroid hormone. In this, Amphibia
agree with mammals. During the breeding season there is a
distinct rise of the metabolic rate which is most marked in the
male (Cronheim, 1927). Metabolism decreases with age. It is
noteworthy that animals which differentiate early and reproduce
at a small size probably never reach the age of the slow-growing,
less differentiated types. At least the large perennibranchs

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 435

and derotremes have longer life records than any of the smaller
Amphibia and the same relation between slow growth and age
seems to maintain for higher vertebrates.

Although the metabolism of Amphibia differs from that of
higher vertebrates in quantity rather than in kind, there is also
the important distinction that warm-bloodedness has made
possible a complex series of interlocking physiological systems
which usually prohibit any marked slackening of the pace of
living without bringing disaster. Thus, while both frogs and
salamanders are known to have lived over a year without food,
and frogs, at least, to have recovered after ice had formed in
their blood and lymph spaces, no warm-blooded type could
resist such adversities. Although Amphibia are deficient in
nervous and other mechanisms which give the mammals the
optimum conditions of energy transformation and body activity,
they can subject themselves to far greater changes of their
metabolic rate and survive. Few, however, can live at the high
body temperatures found in mammals and birds. There is thus
not only a difference in average level but in optimum temperature
levels between Amphibia and higher forms.

Effect of the Environment. — Amphibia possess numerous
structural and physiological adaptations which help them to
live in particular environments. As discussed in a previous
chapter (page 86), these have arisen for the most part by the
gradual selection of favorable mutations by particular environ-
ments. All Amphibia are able to undergo certain adjustments
during development and in some cases this influence of environ-
ment during ontogeny may be considerable. It is frequently
possible to predict the habitat of a species merely by examining a
specimen superficially. Thus, a frog with large adhesive discs
on its toes is usually arboreal; a salamander with a broad tail fin,
aquatic; or a toad with enlarged " spades" on its feet, fossorial.
Numerous instances of such correlations have been given in the
preceding chapters. On the other hand, two closely related
species may have very different habits without showing correlated
differences in structure. The common Amby stoma tigrinum
may remain in the ponds during the summer months (Hay,
1892), while the related A. maculatum which does not seem exter-
nally less fitted for aquatic life is terrestrial throughout the greater
part of the year. The tadpoles of Rana clamitans are vegetarian,
those of R. sylvatica carnivorous (Hay, 1892), but the two species

436

THE BIOLOGY OF THE AMPHIBIA

exhibit only slight differences in their dentition. Hyla arenicolor
has a strong predilection for the vicinity of streams and yet does
not appear better adapted for this habitat than H. versicolor
or many other arboreal species. One would hardly guess from
an external examination that Pseudobranchus burrows in the
mud at the bottom of ponds while the closely related Siren never
exhibits these proclivities. In brief, many habitat preferences
of Amphibia are not reflected in any external characters.

In the chapters dealing with the various organs of Amphibia,
frequent reference has been made to the ontogenetic effects of
environmental factors. The form of the gill, for example, may
be greatly influenced by the amount of oxygen available ; not only
are the gills of Salamandra and newts longer in water poor in
oxygen but their epithelium is much thinner than that on the
gills of larvae retained in the water rich in oxygen (Drastich,
1925). Similarly, Doms (1915) showed that the size and arboriza-
tion of the external gills of Rana esculenta tadpoles increased with
the temperature. It would appear probable that the environ-
ment during each ontogeny would have an influence on controlling
the length of the gills in all Amphibia, although to what extent
it is responsible for the many extraordinary types of gill form
discussed in Chap. Ill is at present uncertain. The effect of the
environment may not only be specific for certain tissues, but it
may also be general on many parts of the body. It is this latter
type of effect which may be dealt with in further detail here.

A decrease of available oxygen lowers the respiratory quotient
in spite of the increase in respiratory surface. This is apparently
due to the accumulation of the products of incomplete oxidation
(Drastich, 1925). It also leads to a decrease in thyroid size
and a slowing up of both development and differentiation. An
increase in the temperature leads to a hypertrophy of the gills
and a thinning of their epithelium apparently in correlation with
the increased gas exchange. At the same time an increase in
temperature leads to a decrease in the size of the body cells and
their nuclei (Hartmann, 1922). A rise in the temperature
increases the metabolic rate of Amphibia, and this in turn has
many effects. The nitrogen excretion of frogs increases with a
rise from 21 to 31°C. At the higher temperature a yellow pig-
ment appears in the urine (Van der Heyde, 1921). The quantity
of food the newt will take increases with the temperature and
this influences directly the rate of growth (Springer, 1909). If

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 437

the maximum quantity of food a newt will take at a low tempera-
ture be taken as a feeding basis, the rate of growth diminishes with
an increase in temperature because the individuals at the higher
temperatures are underfed. It has frequently been noted that
tadpoles, when crowded, do not grow so rapidly as others less
confined. Adolph (1929) has shown that this is not due to the
lack of oxygen but merely because the physical disturbances of
crowding prevent the tadpoles from eating as much as those in
larger ranges. Similarly, axolotls and pond tadpoles accustomed
to feed in quiet water grow more slowly in running water (Goetsch,
1928). This may be due to the fact that such larvae do not
secure enough food or possibly to the fact that they are forced
to use their food reserves more quickly. Among frogs in general,
pond life has produced more giant tadpoles than stream life.
The correlation is not, however, so close among the urodeles.

One of the most remarkable modifications attributed to dif-
ferences in feeding is reported by Powers (1907) in Amby stoma
tigrinum. He found that cannibal individuals differed remark-
ably in their elongate teeth, flat heads, and body proportions
from non-cannibals of the same species. Special diets may lead
to malformations of the tail or body in other salamanders (Klatt,
1927). Overfeeding with liver frequently leads to distended
bodies and bent tail in both larvae and adult salamanders. A
lack of minerals in the diet may produce a curvature of the
spine and a reduction of pigmentation in larval Ambystoma, also
peculiar twists in the tail of the adult (Patch, in press). Feeding
European newts on a shellfish diet (Sphaerium) causes them to
develop with a much shorter head than plankton-fed controls.
Krohn (1930) attributes this change of head form primarily to
an increase in the fluids of the brain ventricles. A one-sided diet
is therefore to be avoided under laboratory conditions where
healthy animals are required. The best initial food for Amby-
stoma larvae is an assortment of small aquatic Crustacea, while
earthworms containing considerable mineral matter should be
added to a diet of beef or liver at a later stage. Whether or not
peculiar diets have produced distinctive types in nature is
unknown. The experiments of Powers have not been repeated
by later investigators and his conclusions are in need of further
confirmation. The question of the inheritance of these and other
environmental effects has been considered in previous chapters.

438 THE BIOLOGY OF THE AMPHIBIA

Microscopic Parasites. — Amphibia suffer the depredations of
many kinds of parasites (Jacob, 1909) some of which are highly
pathogenic, producing diseases which resemble those of man.
The newt picks up more parasites during its aquatic than during
its terrestrial stage (Holl, 1928a). Further, the Cricket Frog,
Acris, is more parasitized during the breeding season when it is
largely aquatic than later in the season. Still, there is no definite
evidence that disease has played a large part in controlling the
distribution of any species of amphibian.

Several species of fungus are known to attack the skin and
intestines of Amphibia. Saprolegnia forms pale, feltlike blotches
over the skin of both frogs and salamanders, especially under
laboratory conditions. Scott (1926) describes a Monilia which
also forms felty growths on the skin of frogs, toads, and sala-
manders. The disease is highly contagious and usually fatal.

One of the commonest bacterial diseases of frogs in captivity is
known as "red leg." This is caused by Bacillus hydrophillus
fuscus, which produces a congestion of the blood vessels on the
ventral surface of the body resulting in more or less hemorrhage
beneath the skin. The frog becomes oedematous and if kept in
water gains in weight due to the absorption of water through the
skin without a compensatory release of water by the kidneys
(McClure, 1925). The disease is usually fatal unless the frogs
are kept at low temperatures for a period.

Other bacteria have been described from frogs (Stutzer, 1926),
including the tubercle bacilli (Lichtenstein, 1920), but it is chiefly
the Protozoa which infest Amphibia in great numbers. The
intestines of frogs and salamanders are inhabited by many species
of flagellates, infusorians, rhizopods, and sporozoans (Collin,
1913).

Hegner (1923) found that living flagellates of the Euglena type
were the normal inhabitants of the intestines of tadpoles living in
ponds rich in algae. Other flagellates, such as Trypanosoma, are
frequently found in the blood of frogs and salamanders. Although
it is a Trypanosoma which produces the African sleeping sickness
and some species such as T. inspinatum are pathogenic in frogs,
other species of the same parasite are not known to have serious
effects upon their host. Some Trypanosomes are transmitted
by leeches, the organisms gaining access to the wound made by
the proboscis of the leech (Wenyon, 1926). The common newt,
Triturus viridescens, is so frequently infected by Trypanosoma

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 439

diemyctyli (Fig. 138) that it may be used as a ready source of
supply for class-room demonstration of this parasite (Hegner,
1920).

The integument of aquatic Amphibia frequently supports a
rich protozoan fauna. Wenrich (1924) reports one flagellate and
seven ciliates from the skin of tadpoles, and Sassuchin (1928)
has added a list of species which he has found in the slime of the
tadpole skin. Under laboratory conditions Cryptobranchus

Fig. 138. — Trypanosoma di- Fig. 139. — Opalina ranarum, a ciliate parasite
emyctyli. (After Nigrelli.) of frogs. (After Metcalf.)

frequently develops a rich growth of Vorticella, and various free-
swimming ciliates may be found in the mucous secretion of the
integument. These in themselves do not appear to be patho-
genic but they are often accompanied by a growth of mold which
causes great injury.

Among the ciliates in the intestines of tadpoles and frogs the
opalinids are perhaps the most common. These have a ciliated
body, several nuclei, but no mouth. Although they may reach
a diameter of nearly a millimeter, they apparently do little dam-
age to the body of their host. Opalinids (Fig. 139) are found in

440 THE BIOLOGY OF THE AMPHIBIA

many parts of the world and have been recorded from fish and
salamanders as well as from frogs. Many species are common
to several families of frogs, but Metcalf (1929), who has recently
monographed the group, believes the distribution of the various
genera lends support to his views of the migration routes of the
frogs and toads which they parasitize. Thus, Zelleriella, which
infests various genera of not closely related frogs, is found nowhere
except in Australia and South and Central America. To Harri-
son and Metcalf this means that South America and Australia
have been joined in past time in some way which excluded north-
ern land masses. It may well be, however, that the northern
opalinids were not in existence at the time the present southern
opalinids were being carried south by whatever species they
happened to parasitize at that time. The host -parasite method
may be used in elucidating the relationships of hosts when the
parasites are specific and when the same or closely related species
are found in two animals of doubtful affinities. But the opalinids
are not specific and they do not help in suggesting either the
relationships of the various genera of frogs and toads or the
migration routes which these genera followed in the past (Noble,
1925).

The Rhizopoda include many of the most common fresh-water
Protozoa. They possess neither flagella nor cilia like the forms
previously considered but move about by projections from the
body called "pseudopodia." The amoeba is the most familiar
example. Dysentery is produced by certain rhizopods, but
whether the several genera described from the intestines of frogs
and newts cause similar diseases in their amphibian hosts is not
known.

The most characteristic parasitic Protozoa of Amphibia are the
Sporozoa. They have neither cilia, flagella, nor pseudopodia and
reproduce mainly by the formation of spores in great numbers
at one time from their one-celled body. Sporozoa have been
recorded from the kidneys, digestive tract, and various other
organs of Amphibia. Guyenot and Ponse (1926) have described
a species from the cells of Bidder's organ in the toad. The
Hemosporidia live in the blood, certain species causing malaria
and tick fever in mammals. Other species occur in the blood of
Amphibia (Sanders, 1928) and certain of these are transmitted
by the bite of a leech (Cleland and Johnston, 1910). Hemospori-
dia while found in the blood of all vertebrates are especially

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 441

abundant in the cold-blooded groups including fishes and reptiles,
as well as Amphibia. Lankesterella is found in the red blood cells
of frogs and is only about half the length of these corpuscles.

Larger Parasites. — Turning to the parasites which one may
more readily see, the roundworms and flatworms are by far
the most abundant. Nematodes, which include the notorious
hookworm of the Southern states, are found in both digestive tract
and body cavity of frogs and salamanders. Acanthocephali,
which are closely allied to Nematoda but have hooks on the pro-
boscis, have been recorded from the intestine of frogs. The
Trematoda, or flukes, are parasitic flatworms still possessing an
alimentary tract but having suckers or adhesive organs. The
most frequently seen is Polystomum, which has a circle of distinct
suckers at the posterior end of the body. It is a common inhabit-
ant of the urinary bladder of frogs. Trematodes are also found
in the intestines of both frogs and salamanders and new species
have recently been described from American forms (Cort, 1919;
Holl, 1928a). Cestodes, which include the tapeworms, represent
the most extreme specialization for parasitic life among the flat-
worms. They are white and segmented. Tapeworms have
been found in the intestines of both European and American frogs.
In addition to round- and flatworms, other wormlike parasites
have been recorded from frogs, including a true oligochaete para-
sitic in the urogenital system of a South American tree frog
(Michaelsen, 1926).

Under laboratory conditions salamanders are sometimes
infested by a red mite which may cause annoyance both to the
salamander and to the observer who wishes to keep the sala-
manders in good health. Flies of several genera parasitize frogs
and toads. Some species lay their eggs in the nostrils of toads
and the larvae which emerge make their way into the nasal
chamber and other parts of the body. Batrachomyia was
described as a genus of flies, the larvae of which lie between skin
and muscle of Australian frogs and, while producing enormous
lumps in the skin, eventually escape without destroying their
host (Skuse, 1889).

In the laboratory the infections of Amphibia frequently cause
considerable inconvenience to the student. Weak solutions of
potassium permanganate, mercuro-chrome, copper sulphate, and
iodine have been used with varying success to remove molds and
external parasites. Pennies kept in the aquaria usually release

442

THE BIOLOGY OF THE AMPHIBIA

enough copper salts into the water to discourage the growth of
molds. Amphibia weakened by disease will sometimes recover
when placed for short periods in the ice box. The use of running
water and the isolation of infected animals will frequently check
the spread of the more common diseases.

Other Enemies. — Frogs and salamanders are harassed through-
out life by legions of enemies and only a very small proportion of
any one brood lives to reach maturity. Although the eggs are
surrounded by a protective jelly, they are frequently eaten or
destroyed, even some salamanders such as the newt, being respon-
sible for some of the losses. Giant water bugs, dragonfly nymphs,
larvae of water beetles, and many other aquatic insects destroy
tadpoles in great numbers. Many microscopic Crustacea attack
salamander larvae, devouring first their gills. Fish, especially
pike, bass, and catfish, prey upon tadpoles and young frogs.
These formidable enemies frequent the larger ponds, which are
usually avoided by Ambystoma during the breeding season but
may form the regular breeding grounds of toads and several
species of Rana. Large frogs will seize smaller individuals of
their own or other species. This cannibalistic habit has been
one of the factors which has led some frog culturists to abandon
the rearing of bullfrogs for market (Wright, 1920). Salamander
larvae frequently devour smaller individuals of the same or dif-
ferent species. This struggle for existence, larva against larva,
has been recorded also among the tadpoles of frogs. De Villiers
(1929) found that tadpoles of the South African Rana grayi
frequented the same pools as the tadpoles of a brevicipitid Cacos-
ternum. As the pools began to dwindle, only the Rana tadpoles
survived. Direct observation in the laboratory showed that
the Rana tadpoles would swallow the Cacosternum tadpole at a
single gulp and this voracious habit was the apparent reason for
the non-survival of Cacosternum under conditions of crowding.
This case is by no means unique. Larvae of some species of
Ceratophrys and Rana are also cannibalistic.

The greatest enemies of frogs are, probably, the snakes. Water
snakes and garter snakes devour many of the smaller species.
The spreading adder, Heterodon, feeds largely on toads and there
are exotic snakes which are known to include a very high percent-
age of toads in their diet. Black snakes, copperheads, and various
other local species have been shown to feed on terrestrial Salientia.
Salamanders, because of their secretive habits, probably suffer

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 443

less than frogs from the depredations of serpents. Other reptilian
enemies of Amphibia include the aquatic turtles. In the United
States the musk and snapping turtles are especially destructive of
tadpoles and may seize frogs. Alligators are also reported to
be foes of frogs. None of these species compares with snakes in
their continuous persecution of the frog tribe.

Birds and mammals take a very high toll of amphibian life.
Ponds abounding with newts and tadpoles have been picked clean
of amphibian life by domestic ducks within a short time after
their release in the area. Herons are well known to stalk the
shallows in search of frogs or their tadpoles. Such a nocturnal
and secretive salamander as Plethodon cinereus was found by
Allen to be captured in some numbers by screech owls. The
common crow was shown by Barrows to take frogs and toads
more regularly than any other kinds of food. The mammalian
enemies are less numerous than birds but include many familiar
forms, such as weasels, skunks, and even rats and cats. Man, by
draining the marshes and by collecting great numbers of frogs at
all seasons, is rapidly exterminating frogs and toads from many
parts of the country. The automobile has been considered the
greatest enemy of the toad, and certainly the pollution of streams
in the Alleghanies has done much to destroy the breeding grounds
of Cryptobranchus. In many indirect ways man makes living
precarious for Amphibia.

Length of Life. — The span of life attained by Amphibia is not
known with certainty. A few species, however, have been in
captivity for long periods. Wolterstorff (1928) records a Japa-
nese newt, Triturus pyrrhogaster, which had been living in his
possession for 25 years, and Debreuil (1925) a Spanish newt,
Pleurodeles waltl, which had lived 20 years without leaving an
aquarium. Common European toads have been credited with
36 years of life, and tree toads with 10 (Szabo, 1927) to 22 years.
Of course the story that a toad can live for centuries entombed in
stone or in old wells is sheer fable. The question was settled as
long ago as 1777 by direct experiment, but the belief is still
prevalent among many people.

In general, larger animals live longer than smaller ones (May-
enne, 1924). A specimen Megalobatrachus maximus, the largest
salamander, has been kept 52 years in the Amsterdam aquarium.
At this time it had reached the length of 114 cm., while a ten-year-
old Siren was only 50 cm. long. Siren has been reported to live

444 THE BIOLOGY OF THE AMPHIBIA

25 years in captivity and Amphiuma 26. In general, the larger
frogs and toads reach sexual maturity later than the smaller
species. Larval life may last less than a month, as in the case of
some Spade-foot Toads, Scaphiopus, to over 2 years, as in some
Bullfrogs. Thoroughly aquatic Salienta, such as the Bullfrog,
Rana catesbeiana, or the South American species, Batrachophrynus
microphthalmus and Pseudis paradoxa, have a longer larval period
(or at least reach a larger larval size) than more terrestrial forms.
Large size is definitely correlated with an abundant secretion of
the hormone from the anterior lobe of the pituitary gland. Fur-
ther, the onset of metamorphosis is induced by the release of the
colloid in the thyroid gland. Possibly the endocrine organs
control the span of life by hastening or slowing up the rate at
which both larval and adult differentiations take place.

Although some newts, Triturus viridescens, and Tiger Salaman-
ders, Amby stoma tigrinum, may become sexually mature as
larvae, most salamanders and frogs do not breed until a year or
more after metamorphosis. Gadow (1901) records axolotls
as becoming sexually mature at about six months of age, and cer-
tain European newts have been reported to reach sexual maturity
in less than a year. Both Plethodon cinereus (Blanchard, 1928)
and Batrachoseps attenuatus (Storer, 1925) reach sexual maturity
2 years after hatching, although they may not breed until nearly
a year later. The tree frog, Hyla arenicolor, breeds when two
years old. Storer (1925) found that of the western toads, Bufo
boreas halophilus required 2 years, Bufo canorus 3 years, and
Bufo cognatus 4 years to reach sexual maturity. This represents
the range found in most frogs, although some species of Rana have
been credited with even greater time to attain sexual maturity.

Age is determined by measuring all the individuals found in a
single locality and plotting the sizes. If enough individuals are
considered, the frequency modes may give the number of years
required to reach sexual maturity, but they will not show the
total age, for most species grow slowly, if at all, after reaching
sexual maturity. Many species, particularly some tropical forms,
seem to have an absolute size which the males soon attain, but
this does not hold for many salamanders nor for some northern
frogs.

References

Adolph, Edward F., 1929: The quantitative effect of crowding on the rate
of growth of tadpoles, Anat. Rec, XLI V, 227.

RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 445

Athanasiu, J., 1899: tjber den Gehalt des Froschkorpers an Glykogen in
den verschiedenen Jahreszeiten, Arch. ges. Physiol., LXXIV, 561-569.

Blanchard, F. N., 1928: Topics from the life history and habits of the red-
backed salamander in southern Michigan, Amer. Naturalist, LXII,
156-164.

Cleland, J. Burton, and J. Johnston, 1910: The haematozoa of Australian

batrachians, No. 1, Sydney, N. S. W., Jour. Roy. Soc, XLIV, 252-260.
Collin, Bernard, 1913: Sur un ensemble de Protistes parasites des batra-

ciens, (Note Preliminaire), Arch. Zool. Exp., LI, 59-76.
Cort, W. W., 1919: A new distome from Rana aurora, Univ. Cal. Pub.

Zool, XIX, 283-298, 5 pis.
Cronheim, Walter, 1927: Gesamtstoffwechsel der Tiere; III. Kaltblutige

Wirbeltiere (Poikilotherme); B. Amphibien und Reptilien, Carl

Oppenheimer's Handb. Biochem. Mensch. Tiere, VII, 329-340.
Davenport, C. B., and W. E. Castle, 1895: Studies in morphogenesis; III.

On the acclimatization of organisms to high temperatures, Arch. Entw.

mech., II, 227-249.

Debreuil, C, 1925: [Note], Bull. Soc. Nat. Acclim. France, LXXII, 155-156.
Dolk, H. E., and N. Postma, 1927: tjber die Haut — und die Lungenatmung

von Rana temporaria, Zeitschr. vergl. Physiol., V, 417-444.
Doms, H., 1915: tjber den Einfluss der Temperatur auf Wachstum und

Differenzierung der Organe wahrend der Entwickelung von Rana

esculenta, Arch. mikr. Anat., LXXXVII, 60.
Drastich, L., 1925: tjber das Leben der Salamandra Larven bei hohem und

niedrigem Sauerstoffpartialdruck, Zeitschr. vergl. Physiol., II, 632-657.
Gadow, H., 1901: "Amphibia and Reptiles," Cambridge Nat. Hist., VIII.
Garten, S., and W. Sulze, 1913: tjber den Einfluss niederer Temperatur

auf die Nerven eines tropischen Kaltbluters (Rana hexadactyla),

Zeitschr. Biol, LX, 163-185.
Goetsch, W., 1928: Untersuchungen iiber wachstumhemmende Factoren,

Zool. Jahrb., Alg. Zool Phys., XLV, 799-840.
Guyenot, Emil, et K. Ponse, 1926: Une Microsporidie, Plistophora

bufonis, parasite de l'organe de Bidder du crapaud, Rev. Suisse Zool,

XXX, 213-250.

Hall, F. G., and R. W. Root, 1930: The influence of humidity on body
temperature of certain poikilotherms, Biol. Bull, LVIII, 52-58.

Hartmann, Otto, 1922: tjber den Einfluss der Temperatur auf Grosse und
Beschaffenheit von Zelle und Kern im Zusammenhang mit der Beein-
flussung von Funktion, Wachstum, und Differenzierung der Zellen
und Organe (Experimente an Amphibien), Arch. Entw. Mech., XLIV,
114-196.

Hay, O. P., 1892: The batrachians and reptiles of the state of Indiana, Ind.

Dept. Geol Nat. Resources Ann. Repl, 1891.
Hegner, R. W., 1920: Blood inhabiting protozoa for class use (Trypanosoma

diemyctyli), Science, LI, 187-188.
, 1923: Observations and experiments on Euglenoidea in the digestive

tract of frog and toad tadpoles, Biol. Bull, XLV, 162-180.
Helff, O. M., 1927: The rate of oxygen consumption in five species of

Amblystoma larvae, Jour. Exp. Zool, XLIX, 353-361.

446

THE BIOLOGY OF THE AMPHIBIA

Hill, A. V., 1911: The total energy exchanges of intact cold blooded

animals at rest, Jour. Physiol., XLIII, 379-394.
Holl, F. J., 1928: Parasites of North Carolina amphibians, Jour. Elisha

Mitchell Sci. Soc, XLIV, 20.
, 1928a: A new Trematode from the newt Tri turns viridescens, Jour.

Elisha Mitchell Sci. Soc, XLIII, 181-183, 1 pi.
Isserlin, M., 1902: tjber Temperatur und Warmeproduction poikilo-

thermer Tiere, Arch. ges. Physiol., XC, 472-490.
Jacob, E., 1909: Zur Pathologie der Urodelen und Anuren, Zool. Anz.,

XXXIV, 628-638.

Kenyon, W. A., 1925: Digestive enzymes in poikilothermal vertebrates;
An investigation of enzymes in fishes, with comparative studies on
those of amphibians, reptiles and mammals, Bull. Bur. Fish. Wash.,
XLI, 181-200.

Klatt, B., 1927: Futterungsversuche an Tritonen; II. Die Bedeutung der

Ausgangsgrosse, Arch. Entw. Mech., CIX, 176-187.
Krogh, A., 1916: "The Respiratory Exchange of Animals and Man,"

London and New York.
Krohn, E., 1930: Futterungsversuche an Tritonen; III. Die Veranderung

der Kopfform des Teichmolches (M. vulgaris [taeniata]) infolge

Muschelfleischfutterung, Arch. Entw. Mech., CXXI, 545-597.
Laurens, H., 1914: The influence of temperature on the rate of the heart

beat in Amblystoma embryos, Amer. Jour. Physiol., XXXV, 199-210.
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Zool. Anz., LXI, 235-237.
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with special reference to the oedema in red-leg disease, Amer. Anat.

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Metcalf, M. M., 1929: Parasites and the aid they give in problems of
taxonomy, geographical distribution and palaeontology, Smithson.
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Michaelsen, W., 1926: Schmardaella lutzi Mich., oligochaeto endopara-
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4 pis.

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RELATION OF AMPHIBIA TO THEIR ENVIRONMENT 447

Skuse, F. A. A., 1889: Description of a new genus (Batrachomyia, W. S.

Macleay M. S.), and two species of dipterous insects, parasitic upon

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Fish. Doc. 888, App. VI, Rep. U. S. Comm. Fish., 1919.

CHAPTER XIX

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE

The distributions of the various groups of Amphibia are con-
sidered in some detail in the second part of this volume. It is,
however, of some interest to compare distributions and to
attempt to determine the probable routes of dispersal of each
family. Such conclusions, if sound, should be in harmony with
the conclusions of zoogeographers studying other groups of land
animals of the same apparent age.

Geographical Distribution. — It is a well-known fact that the
various groups of Amphibia show different geographical distribu-
tions. Urodeles are found primarily in the northern hemisphere,
caecilians are circumtropical, while frogs and toads occur over
the entire world except in regions of extreme cold or aridity.
The various families have also different limits of distribution.
Hynobiid salamanders are found only in Asia and adjacent
islands; ambystomids, amphiumids, and sirenids only in North
America. The small family of Cryptobranchidae have repre-
sentatives living today only in Japan, China, and eastern North
America; the Proteidae, only in Southern Europe and eastern
United States. The salamandrids, with their center of maximum
abundance of species in Europe, are widely spread in the northern
hemisphere, while the Plethodontidae, the dominant group of
North American salamanders, have two species in southern
Europe and a few in the Andean region of South America. The
Salientia have equally distinctive ranges,: the Liopelmidae live
today only in New Zealand and northwestern United States;
the Discoglossidae, in Europe and Asia including the Philippines.
The Pipidae are found in the tropics of Africa and South America;
the Pelobatidae are holarctic but have invaded the tropics in the
Philippines, the East Indies, and the Seychelle Islands. The
small family of brachycephalid toads is confined to the neotropics.
The large families of bufonids, hylids, ranids, and brevicipitids
are distributed over most of the continents but do not have
identical ranges. The Hylidae exhibit a broad hiatus in the

448

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE 449

IndoMalayan region, while the Ranidae are absent from South
America except for Rana which has reached only the northern
part of the continent.

The ranges occupied today by the urodeles do not coincide with
those of the frogs; the geographic limits of each family of
Amphibia have their own peculiarities. These differences are due
to the different times at which the groups arose in the past, the
different modes of living, and the different barriers which affected
the dispersal of the groups. If a natural group of Amphibia today
occupy two distinct territories, species of this group must at some
previous period have lived in the intervening area. Unfor-
tunately, Amphibia do not make good fossils and there is very
little record of the ancient wanderings which must be postulated
to account for present distributions.

Some reference may, nevertheless, be made to this meager
record, for it is a fair index of the kinds of migration which
occurred. Although the Cryptobranchidae are thoroughly aquatic
urodeles, living today only in streams, they had during the latter
part of the Tertiary a very wide distribution (Fig. 140). Fossil
cryptobranchids are known from the Miocene of Europe and the
Lower Pliocene of Nebraska, and hence the group formerly flour-
ished in regions where today no living individuals occur. Simi-
larly, the primitive salamandrid Tylototriton is confined today to
the eastern Himalayas, Yunnan, Burma, and the Riu-Kiu Islands,
but it also is known as a fossil from the Miocene beds of southern
Europe. There are other definite cases, such as that of Spade-
foot Toads from the Oligocene of Mongolia and the extinct
family of toads, Palaeobatrachidae, from the Oligocene and
Miocene of Europe, which show conclusively that amphibian
faunas have existed in regions now devoid of these forms. They
also show that groups which have passed through a region need
not have left relic types behind as proof of these migrations.

The present distribution of the various groups of Amphibia
demand that land connections existed in previous times between
regions now separated by water. Europe and America were
apparently connected, it would seem by way of Greenland, at a
time when this northern region enjoyed a warmer climate. The
European Proteus and the American Necturus are closely related
and the only members of the distinct family Proteidae. The
plethodontid genus Hydromantes has one species in the Sierra

450

THE BIOLOGY OF THE AMPHIBIA

A second land bridge, frequently postulated to explain the
distribution of higher groups such as the mammals, connected

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE 451

Alaska and Asia. It was apparently across this bridge that
Cryptobranchus, Ascaphus, and the brevicipitids came from
Asia. The narrow-mouthed toads included at least Microhylinae
and Kalophryninae in their original migratory stock, for repre-
sentatives of both subfamilies are now in China and the United
States. The north-Pacific land bridge probably admitted pelo-
batids and some of the hylids to America; but here the evidence
is not so conclusive.

Land Bridges. — The distribution, both present and past, of the
Amphibia does not demand any other land bridges across the
Atlantic or Pacific than those just indicated. Geologists have
shown the extensive changes in elevation which have taken place
on the continental masses. North and South America have been
at various times connected and disconnected; further, there was,
during parts of the Tertiary, less water between Asia and Aus-
tralia than now exists. Apparently, the Amphibia made exten-
sive migrations along these land masses. During the Mesozoic,
Dinosaurs existed on all the continents ; while during the Tertiary,
various groups of mammals migrated over the greater part of the
world. Salientia were in existence since Jurassic times at least,
and it is not improbable that hylids and bufonids were established
in the southern hemisphere before the beginning of the Tertiary.
The frog faunas of South America and Australia have con-
siderable resemblance. In both, bufonids and hylids are domi-
nant types. This does not necessitate our assuming that these
two continents must have been connected. It has recently been
shown that toothed bufonids closely allied to Crinia of Australia
existed in the Eocene of India (Noble, 1930). The bufonids of
Australia are as closely related to the African forms as they are to
the South American species. Hyla is found in Australia and
South America, but this genus has been described as a fossil
from the Miocene of Europe. When the world-wide distribution
of the hylids and bufonids is considered, it becomes clear that both
of these families in all probability arose in the north and spread
southward along existing continental masses to their present
ranges (Noble 1925). This retreat to the South is no more
remarkable than that which our knowledge of fossils shows us
to have taken place in many other groups, as, for example, in the
pleurodire turtles.

There are many peculiarities of distribution for which we have
at present no adequate explanation. Thus, pelobatids are now

452

THE BIOLOGY OF THE AMPHIBIA

known from the Seychelle Islands but none from Africa. Were
the Seychelle Islands formerly connected with India where
pelobatids live today, or did pelobatids in former times abound
in Africa? Toothed brevicipitids occur in Madagascar and
southern Asia. The tree frog, Polypedates, is common to both
regions. Is this evidence that Madagascar and Asia were con-
nected? Madagascar lacks the pipids, bufonids, and caecilians
of Africa, a fact which suggests a long isolation from the African
mainland, but this region includes the modern and characteristi-
cally African Hyperolius and Megalixalus, which seems to indi-
cate that frogs have been able to reach that island in recent times.
From such data as these it seems probable that Madagascar may
have been always separated from Africa but that long ago it
received by flotsam-jetsam methods a few brevicipitids and
ranids which underwent a remarkable radiation on that island.
Similarly, the connection between Australia and Asia may never
have been entirely complete in order to have admitted the few
types of Salientia which underwent a specialization there.

Age and Area. — In determining the migration routes of animals
it is important to know the relative age of the group and the
methods of dispersal available to it. If the group is a compara-
tively modern one in which few extinctions have occurred, the
center of dispersal will tend to lie near the center of the group
range, at the intersection of the possible routes of migration.
The oldest groups will tend to have the widest distribution and,
because of the frequency of extinction, will also exhibit the
most discontinuous ranges. This rule seems to hold for liopel-
mids and pipids but not for some other presumably ancient
groups such as the hynobiid salamanders.

Most animals, including the Amphibia, gradually extend their
ranges in the course of their normal wanderings. Nevertheless,
the various species are usually restricted in their travels to dis-
tinctive habitats. This is not always the case, since various
aquatic species have been known to make long overland journeys
after rains. The dispersal of animals is augmented by the
climatic cycles which bring profound changes in the environments
of any one locality. When such changes occur, any animal with
restricted habitat requirements must move out in order to survive.
It was the recognition of this fact which led Matthew (1915)
to conclude that the primitive forms of any group will in general
be found on the periphery of the range, for most groups have

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE 453

survived one or more of these climatic cycles and have left the
original home territory to more advanced types adapted to meet
the new conditions. The rule does not apply to all groups of
Amphibia. Some, such as the Plethodontidae, may have arisen
in a region which has not undergone a marked change (Dunn,
1926) and the specialized derivatives of the original stock may
be found anywhere throughout the range where habitat condi-
tions permit.

Barriers to Dispersal. — The requirements of Amphibia, so
important in limiting their migrations, vary with the species.
Ascaphus thrives at temperatures a few degrees above freezing
and dies in captivity unless kept cool. The smooth-skinned
Bufo alvarius can live successfully only near streams, while its
rough-skinned relative B. cognatus is at home in the desert. All
Amphibia demand some moisture, but as this requirement
varies with the species, due to the inherited morphological and
physiological peculiarities of the form, the moisture content of
any one locality may determine the species living there.

As in the case of fishes and birds, the distribution of Amphibia
is often limited by their breeding-site preferences. Frogs or
salamanders which lay their eggs near mountain streams usually
do not wander far from these locations. Necturus is found more
commonly in streams affording nesting sites than in those lacking
a bed of suitable stones. On high mountains, such as the Andes,
a large part of the frog fauna consists of species which skip over
an aquatic larval stage and the only salamanders in the Andes,
at least, are ovo viviparous species. Similarly, in rain forests such
as those in Jamaica the frogs are species which avoid an aquatic
stage or are forms with larvae adapted to living in the small
amounts of water caught between the leaves. No doubt the
direct development of Eleutherodactylus has been one of the
principal factors in making this group of frogs one of the com-
monest in the neotropics. Again, in the deserts a premium is
placed not only on species which can dig down to moisture but on
digging forms which are able to undergo a very rapid develop-
ment in the temporary pools left by showers. In brief, both the
restrictions of the habitat for breeding as well as the breeding
preferences of the species have greatly influenced the present
distribution of Amphibia.

Aquarists have noted many times that various alpine species
of salamander can be shipped or kept in captivity only with

454

THE BIOLOGY OF THE AMPHIBIA

difficulty. In the case of Euproctus asper, shallow running water
at ordinary temperatures may be used as a substitute for the
alpine-lake habitat of the species. E. asper has greatly reduced
lungs, and apparently the oxygen requirements hold the species
in waters rich in oxygen. On the other hand, some species of
salamanders may be restricted to particular ranges because of a
special sensitivity to high temperatures. Salamandrina, for
example, in spite of its rough skin will frequently be killed by the
heat of the hand (Klingelhoffer, 1930) and its temperature require-
ments may be the principal reason why it does not extend its
range into the plains of Italy. Many Amphibia may have
requirements difficult to define in physicochemical terms. The
distribution of Aneides lugubris seems restricted to the live oaks in
California (Storer, 1925). Rana clamitans and R. catesbeiana of
the East live and breed in ponds ; Rana boylii and Hyla arenicolor
of the West lay their eggs in the stream habitats which they
frequent throughout the year. Whether it is temperature, mois-
ture, or current which holds the latter forms in these localities is
difficult to say. It may be noted that the higher plethodontids,
such as Plethodon, Hydromantes, and Oedipus, which have given
up an early life in the water, have extensive ranges.

Many factors combine to make an amphibian a successful
migrant. Bufo has a world-wide distribution except for Mada-
gascar, Australia, and most of Polynesia. Toads of this genus
are modern and hence presumably recent travelers. What
makes Bufo a successful type while many far older forms seem on
the verge of extinction? Some toads, such as Bufo boreas
halophilus and B. punctatus, can withstand brackish and highly
alkaline waters (Storer, 1925); others can live in deserts by
digging for short depths underground. Some, such as B.
superciliaris of Africa, are purely forest creatures; while others
of the same region, notably B. regularis, have adapted themselves
to a wide variety of conditions. Hardiness, adaptability, and
aggressiveness may carry an amphibian a long distance in a short
time. The common frog, R. pipiens, is a modern aquatic species
but it has the widest range of any American Rana. It would seem
that agressiveness was an important factor in the distribution of
this species.

Many frogs and toads are found today on islands, especially in
the East and West Indies. It has been assumed that their
presence there indicates that the islands were at one time con-

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE 455

nected with the mainland, but there are other possibilities to
consider. Hurricanes are known to strip trees completely of their
leaves and to transport the contents of ponds for varying dis-
tances ( Visher, 1925) . Eggs could be readily carried in the debris,
and as adult frogs are known to leap successfully from great
heights (Cott, 1926), it is not improbable that they could make
an aerial trip successfully. Storms frequently move against
prevailing winds and hence would transport Malayan forms into

Fig. 141. — Speciation in Plethodon: (A) Plethodon shermani. {B) P. metcalfi.
(D) P. jordani. (E) P. yonahlossee. They inhabit different mountain ranges in
the Southern Appalachians and represent local modifications of the Plethodon
glutinosus stock (C) which covers a wide range in eastern United States.

some of the East Indies and Central American forms to some of
the West Indies. At times of storms, great masses of vegetation
are carried by freshets out to sea. Tree frogs regularly make the
trip in banana shipments from Central America to the United
States and it is highly probable that they could survive a short
sea voyage in a natural raft. Primitive man may have inadvert-
ently carried some of the species. There are many possibilities
and little certainty as to how most of these island Amphibia
reached their present homes.

456 THE BIOLOGY OF THE AMPHIBIA

Frogs and toads are most abundant in the tropics, salamanders
in temperate regions. Still, only two salamanders, an Amby-
stoma and a newt, reach Alaska although a Rana, a Bufo, and a
Hyla occur there. Amphibia are unable to live in regions having
a permanently frozen subsoil, but two species of Rana live north
of the Arctic Circle in Norway and Russia and one salamander
inhabits artic Asia.

Few genera of Amphibia are spread today over more than one
continent, and here their distribution may be confined to certain
environmental niches. Evolution is speeded up by diversity of
environment. With the greater number of ecological niches
that become available, the more chances there are for the isolation
of new types. Hence, mountainous regions with their variety of
habitat types tend to have more genera and species than lowlands
with their uniform vegetation areas. Conversely, the number
of species in a region is usually an index of the degree of environ-
mental diversity (Fig. 141).

Where species are abundant, as in many recent genera of sala-
manders and frogs, it is frequently possible, to trace out the
relationships of the different species and plot these groupings on
their map of distribution. The point where two or more such
plotted groups intersect may be taken as the center of dispersal
from which these related groups of species evolved. Such a
center may not represent the original home of the genus but it will
represent the point from which the species under consideration
probably radiated. Applied to the fauna of the United States,
the method has revealed considerable northern migration.
This very probably followed closely after the retreat of the
Pleistocene glaciers.

Economic Value. — Toads being indiscriminate feeders on insect
life are valuable aids to the farmer in keeping down insect pests.
Frogs swarm in the paddy fields of Japan and China and are
undoubtedly useful in destroying obnoxious insects (Okada,
1927). Frogs and toads are active in the evening and hence
supplement the efforts of birds in retaining the balance of nature.

Frogs' legs form a staple article of food in various parts of the
world. Nearly a million frogs are killed each year in the United
States for their legs (Chamberlain, 1900). Although various
attempts have been made to farm frogs, "no definite successful
mode of procedure has been evolved" (Wright, 1920) and prac-
tically the entire American crop is secured in the wild state. The

GEOGRAPHIC DISTRIBUTION AND ECONOMIC VALUE 457

principal species hunted for their legs are Rana pipiens, R.
catesbeiana, and R. palustris. In New York State the first-
mentioned species is taken most abundantly. As much as 500
pounds of frogs' legs have been netted in a single night by placing
a half mile of cheesecloth screen, supported by sticks and leading
to receptacles, near the shore where it would intercept frogs
migrating to hibernate. Rana pipiens is frequently hunted
in the uplands where this species goes to feed after the breeding
season. Adams and Hankinson (1916) suggest that a frog farm,
to be successful, should provide not only swamps but also
upland feeding grounds where the frogs would be less crowded.
No doubt the natural food in a swamp is not enough to provide
for the large colony which gathers there during the breeding sea-
son. If captive frogs are closely crowded they must be given
additional food. Still, it is doubtful if frogs can be raised in
greater numbers than they are still captured in the wild state.
As many as 150,000 frogs were held by one New York State
dealer during the fall of 1915.

Dried toads and frogs are sold in China as food or for medicinal
purposes (Henderson, 1864). Toad skins have been used in
Japan and elsewhere as a source of fine leather. In Japan dried
salamanders are employed as a vermifuge (Dunn 1923). The
axolotl is sought in Mexico as an article of food. Many super-
stitions have been attached to frogs and salamanders. In parts
of South China the brilliant Polypedates dennysi is worshiped by a
cult and carried about in a chair by faithful members of this group
(Pope, 1931).

One of the most important aspects of frogs and salamanders is
their martyrdom to science. Amphibian larvae afford excellent
material for studying many problems of developmental mechanics
and endocrinology. The frog, especially Rana pipiens, has long
been employed in laboratories of general physiology. Frogs and
salamanders, standing at the base of the tetrapod series, have for
many years been employed as a type form in university instruc-
tion in vertebrate zoology.

References

Adams, C. C, and T. L. Hankinson, 1916: Notes on Oneida Lake fish and

fisheries, Trans. Amer. Fish. Soc, XLV, 154-169.
Chamberlain, F. M., 1900: "A Manual of Fish-culture Based on the

Methods of the U. S. Commission of Fish and Fisheries," rev. ed., U. S.

Comm. Fish and Fisheries, Wash., 252-253.

458

THE BIOLOGY OF THE AMPHIBIA

Cott, Hugh, B., 1926: Observations on the life-habits of some batrachians
and reptiles from the Lower Amazon, Proc. Zool. Soc. London, 1926, II,
1159-1178.

Dunn, E. R., 1923: The salamanders of the family Hynobiidae, Proc.

Amer. Acad. Arts Sci., LVIII, 445-523.
, 1926: ''The Salamanders of the Family Plethodontidae," Smith

College, Northampton, Mass.
Henderson; James, 1864: The medicine and medical practice of the Chinese,

Jour. Roy. Asiatic Soc. N. China Branch, 1, n. s., 21-69.
Klingelhoffer, W., 1930: Terrarienkunde, Lief 15-16, Stuttgart.
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XXIV, 171-318.

Noble, G. K., 1925: The evolution and dispersal of the frogs, Amer. Natu-
ralist, LIX, 265-271.

, 1930: The fossil frogs of the intertrappean beds of Bombay, India,

Amer. Mus. Novit., No. 401.

Okada, Y., 1927: Frogs in Japan, Copeia, No. 158, 161-166.

Pope, C. H., 1931: Notes on Amphibia from Fukien, Hainan and other
parts of China, Bull. Amer. Mus. Nat. Hist., in press.

Storer, T. L, 1925: A synopsis of the Amphibia of California, Univ. Cal.
Pub. Zool., XXVII, 1-343, 18 pis.

Visher, S. S., 1925: Tropical cyclones and the dispersal of life from island
to island in the Pacific, Ann. Rep. Smithson. Inst., 1925, 313-319.

Wright, A. H., 1920: Frogs: their natural history and utilization, Bur.
Fish. Doc. 888, App. VI, RejA. U. S. Comm. Fish., 1919.

PART II

RELATIONSHIPS AND CLASSIFICATION

The frogs, toads, and salamanders include only some 1,900
species and 234 living genera. It is possible to discuss the mutual
relations of these genera without giving a full description of each
group. On the other hand, the fossil Amphibia are based so
frequently upon incomplete skeletal material that only the
broader relations will be considered here. The caecilians rarely
find their way into biological laboratories and a synopsis of the
genera has been omitted from the following account. Those
who have the occasion to study caecilians will find Nieden's
recent review (1913) of their classification useful. The bibliog-
raphy at the close of the chapter includes the principal literature
dealing with systematics of Amphibia.

ORDER 1. LABYRINTHODONTIA. — The labyrinthodonts
or stegocephalians are crocodile- or salamander-like Amphibia
which lived from the Lower Carboniferous to the Triassic period.
As shown by the fossils, they had a skull completely roofed over
with bone. Many more bony elements were present in their
skulls than occur today in modern Amphibia; especially signifi-
cant were an extra row of four bones lying behind the parietals,
several extra bones in the orbit, and a lower jaw consisting of at
least eight pieces on each side. The group receives its name from
the enlarged teeth with greatly folded dentine found in both jaws.
Many species were aquatic, as shown by the well-marked lateral-
line canals on the skulls, but others, such as Cacops, may have
been terrestrial. The suborders or grades of labyrinthodonts are
distinguished primarily by differences in the vertebrae. In all,
the vertebrae consist of neural arches and intercentra; and in
all except the Stereospondyli, a free, ossified pleurocentrum is
present. The various genera in the order have recently been
revised by Watson (1919, 1926) and Romer (1930). The classi-
fication employed for this order is that adopted by Watson.

SUBORDER 1. EmboLOMERI.— The most primitive Amphibia
were the Embolomeri which lived from the Lower Carbon-

459

460

THE BIOLOGY OF THE AMPHIBIA

iferous through the Permian. The centra were double, that is,
the intercentrum and pleurocentrum formed complete rings and
the neural arch attached to one or both of them. The occipital
condyle was single or triple, and a well-ossified basioccipital and
basisphenoid were present. The palate was well ossified, broad
pterygoid bones leaving very small vacuities between them and
the parasphenoid. The various genera in the suborder have been
grouped into the families Anthracosauridae, Loxommidae, Pho-
lidogasteridae, and Cricotidae.

SUBORDER 2. RACHITOML— The rachitomous labyrintho-
donts lived during the Permian and Triassic periods. They
differ from their embolomerous ancestors in that each vertebra
consists of a half-moon-shaped intercentrum and one or two pairs
of pleurocentra in addition to the neural arch. The occipital

Fig. 142.— £ryops megacephalus, a rachitomous amphibian of the North Ameri-
can Permian. Restoration based on mounted skeleton.

condyle was triple or double and the interpterygoid vacuities
wider than in the Embolomeri. The tabulars and dermo-
supraoccipitals in this group form occipital flanges, not present
in the Embolomeri. Watson (1919) recognizes the following fam-
ilies: Eryopidae, Actinodontidae, Rhinesuchidae, Achelomidae,
Dissorophidae, Trematopsidae, Zatrachydae, Archegosauridae,
Trimerorachidae, Lydekkerinidae, Micropholidae, and Dwina-
sauridae. The last mentioned, to judge from its hyoid was
apparently a neotenous group. The best-known rachitomous
amphibian is Eryops (Fig. 142). It attained the length of 4
or 5 feet and resembled an alligator but had a shorter tail.

SUBORDER 3. Stereospondyll— The most advanced sub-
order of labyrinthodonts lived during the Triassic period. They
differed from the preceding in having the centrum formed almost
entirely of the intercentrum, the pleurocentra being rudimentary
or absent. Tendencies found in the Rachitomi are carried to an
extreme in this group. The occipital condyle is double, the basi-

RELATIONSHIPS AND CLASSIFICATION 461

occipital and basisphenoid being reduced. The interpterygoid
vacuities are increased in size and the occipital flanges are more
extensive. Some genera such as Plagiosternum are very broad-
headed and obviously aquatic; others resemble ga vials and
crocodiles in the form of their head. The genera are grouped
into the families Capitosauridae, Trematosauridae, Metoposauri-
dae, Mastodonsauridae, and Brachyopidae.

ORDER 2. PHYLLOSPONDYLI. — The branchiosaurs and
their allies are small, salamander-like Amphibia, found in the
Carboniferous and Permian deposits. They were derived from
the primitive labyrinthodonts and resemble such forms as Eryops
closely in the number and arrangement of elements forming the
skull roof. They are believed to be the ancestors of both the
Salientia and Caudata, although they seem highly specialized in
certain features of their skull and girdles. The vertebrae of the
typical Branchiosauridae are usually described as tubular with
the spinal cord and notochord lying in one cavity. It seems,
however, more probable that the vertebrae were formed epi-
chordally as in Xenopus, the neural arch never growing down
around the notochord. In this case the centrum would be
represented by the thick floor of each vertebral ring. This
conclusion derived from a study of original material received
support in the recent work of Whittard (1930). Some branchio-
saurs appear to have such vertebrae with opisthocoelous artic-
ulations like Xenopus. According to Bulman and Whittard
(1926), the branchiosaurs were adapted to a life in muddy fresh
waters and this is the normal habitat of Xenopus. The branchio-
saurs resembled frogs in their well-marked transverse processes
with short ribs, the cartilaginous pubis, the four fingers and
five toes, and the general configuration of bones forming the
palate. There were pre vomers, palatines, and pterygoids, the
latter narrow and separated by broad, interpterygoid vacuities
from the narrow parasphenoid. A clavicle, cleithrum, and
scapula were present but the coracoid remained cartilaginous
as in some urodeles. Another urodele feature was the three pairs
of external gills carried during a long larval life on broad gill
arches well provided with " rakers" which may have been bony.
The skull roof had a separate quadratojugal, as in frogs, and a
lacrimal, as in some salamanders, for it had not undergone the
loss of elements necessary to convert the skull into that of a
modern amphibian. Although branchiosaurs lost their gills in

462

THE BIOLOGY OF THE AMPHIBIA

adult life, no extensive reorganization of the skull occurred at the
time of this metamorphosis. The occiput was more cartilaginous
than in frogs or salamanders. Both exoccipitals and opisthotics
were present (Whittard, 1930), however, but not so extensive as
in modern species.

Frogs and salamanders may not have sprung from branchio-
saurs but from Phyllospondyli closely related to the Branchio-
sauridae. Other families which have been placed in this order
are the Peliontidae, Colosteidae, Stegopidae, and Acanthostoma-
tidae. The first of these families is intermediate between laby-
rinthodonts and typical branchiosaurs. Labyrinthodont teeth
are present, also an ectopterygoid. The pterygoid articulated
with the anterior margin of the basisphenoid region as in primi-
tive labyrinthodonts, whereas in later branchiosaurs it attached
more posteriorly and dorsally, as in frogs. Romer (1930) refers
some vertebrae to the Colosteidae which were perichordal with a
transverse process springing from the neural arch as in frogs.
Possibly the epichordal and the perichordal types of vertebrae
were already established in the phyllospondyl ancestors of the
Salientia. It is noteworthy that although the epichordal type
of vertebrae characterizes many primitive Salientia, the most
primitive group of Salientia, the Liopelmidae, apparently retains
the perichordal type.

ORDER 3. LEPOSPONDYLL— The small Carboniferous
and Permian Amphibia, which are neither labyrinthodonts nor
Phyllospondyli, may be grouped together in a single order,
although they include several very distinct evolutionary lines.
Most lepospondyls have vertebrae composed of a single piece,
the neural arch being continuous with the centrum which is well
ossified, greatly constricting the chorda. Most lepospondyls
have the ribs articulating with the column intervertebrally, and
this has been considered one of the principal characters separating
lepospondyls from phyllospondyls and their apparent derivatives,
the Salientia and Caudata. In some lepospondyls there is a
secondary shift of the rib to the side of the vertebra. These
lepospondyls are nevertheless readily distinguished from typical
Branchiosauridae by their cylindrical centra.

SUBORDER 1. AdelospONDYLL— In this recently denned
group (Watson, 1926a) the neural arch is joined by suture to a
centrum which has a distinctive form, a pair of depressions
penetrating the ventrolateral surface of each vertebra. The

RELATIONSHIPS AND CLASSIFICATION 463

most advanced member of the suborder isLysorophusof the Lower
Permian of North America, now known in some detail, thanks to
the investigations of Sollas (1920). This genus is frequently
referred to as a " Permian urodele," although it retains too many
labyrinthodont characters to be considered a near relative of the
Caudata.

SUBORDER 2. AlSTOPODA. — Among the Carboniferous lepos-
pondyls were several genera of legless, long-bodied Amphibia
which are grouped here as a distinct suborder. They possessed
elongate skulls, distinctive transverse processes, and peculiar
ribs. They were the sirens and amphiumas of the Carboniferous
swamps; and even at this early time leg reduction had been car-
ried to completion in this one group.

SUBORDER 3. NECTRIDIA. — The skull structure of the more
primitive genera of Nectridia was close to the embolomerous plan.

Fig. 143. — Head of Caecilia tentaculata.

Zygosphene-zygantrum articulations were present on the rather
elongate neural arches. In the more advanced types as repre-
sented by Diplocaulus, the posterior angles of the head are pulled
out to form a peculiar, triangular-shaped head. In spite of this
specialization, Diplocaulus possessed many primitive features
such as a separate coracoid (Douthitt, 1917) and possibly a fifth
finger. All other Amphibia except certain Embolomeri have
lost the outer finger, and hence the retention of this structure in
one suborder of lepospondyls is of interest.

SUBORDER 4. GASTROCENTROPHORI.— The salamander or
Amphiuma-like lepospondyls of the families Microbrachidae,
Hylonomidae, Limnerpetontidae may be grouped together
following the lead of Abel (1919), although their relation to each
other and to the other suborders is not well defined.

ORDER 4. GYMNOPHIONA. — The Gymnophiona or cae-
cilians are limbless, long-bodied Amphibia, living today and
having no fossil representatives. They resemble large earth-

464

THE BIOLOGY OF THE AMPHIBIA

worms, for their bodies are usually provided with a series of trans-
verse grooves. Within these folds are found in many genera a
series of small scales. These are unquestionably an inheritance
from the Carboniferous Amphibia. Other primitive features
are a postfrontal (Ichthyophis), an ectopterygoid (Hypogeophis),
and many features of the gill clefts, hyobranchial apparatus, and
viscera recorded in the above chapters. Although the caecilians
are highly modified for a burrowing life, they retain many very

Fig. 144. — Everted intromittent organ of the male Scolecomorphus uluguruensis.

primitive features, and it seems certain that they originated from
some other group of fossil Amphibia than did the frogs and
salamanders; presumably they arose from lepospondyls. Among
the distinctive features of the caecilians is the protrusible ten-
tacle (Fig. 143) which is found on the side of the face between
nostril and eye of all the species. Their lidless eyes are usually
indistinct and frequently hidden under the bones of the skull.
The males are provided with a protrusible copulatory organ (Fig.
144). One character they possess in common with the frogs is
their short tail, the vent being nearly terminal.

RELATIONSHIPS AND CLASSIFICATION

465

Nieden (1913) recognizes 19 genera and 55 species of caecilians
all belonging to a single family. The more primitive genera such
as Ichthyophis and Rhinatrema possess scales and have the
greatest number of skull elements, while the more specialized
genera have lost the scales and exhibit various fusions of the
skull elements. One genus, Typhlonectes, is aquatic and has
developed a flattened tail. This genus gives birth to its young
alive, while the more primitive genera, such as Ichthyophis and
Rhinatrema, lay large-yolked eggs on land. There may or may
not be an aquatic larval life according to the genus (see Chap.
III). The Gymnophiona are found throughout the tropics but
are absent from Madagascar. They are seldom seen owing to
their burrowing habits.

ORDER 5. CAUDATA. — The salamanders and newts form a
natural group of Amphibia derived from the Phyllospondyli.
They retain many of the characters of their ancestors but have
suffered numerous losses of both cranial and pectoral-girdle
elements (see page 215). All urodeles possess tails, and their
larvae, if aquatic, resemble their parents closely, having among
other features teeth in both jaws. Thus, neither the adult nor
larval urodeles can be confused with frogs, the Salientia, which
apparently arose from the same stock. The adult Salientia
early specialized for leaping and lost their tails. The larvae,
if aquatic, are usually of the polliwog type, or at least never
possess true teeth until metamorphosis.

The name "Caudata" is used today for the order by sys-
tematists. In the herpetological literature there are found other
names for the same group: "Batrachia Gradientia," "Urodela,"
"Saurabatrachia," etc. The history of the early classifications
and the origin of many of these names have been given by Gadow
(1901) and Hoffman (1873 to 1878).

The Caudata are divided into five natural groups or suborders.
The first three: Cryptobranchoidea, Ambystomoidea, and Sala-
mandroidea, converge toward a common ancestor; but the
ancestral stocks of the other two, Proteida and Meantes, are
uncertain. The systematic position of Hylaeobatrachus from
the Wealden formation of Belgium is unknown. It possessed
branchial arches and was obviously of a larval type. Some
authors place this oldest known urodele in a separate family.

Suborder 1. Cryptobranchoidea.— The most primitive
Caudata retain a more generalized skeleton than the other uro-

466

THE BIOLOGY OF THE AMPHIBIA

deles. The angular is free, not fused with the prearticular, as in
the other suborders. The second epibranchial is retained in
the metamorphosed adult. The spine of the premaxillary is
short, not separating the nasals. Certain features of the mus-
culature are apparently distinctive. The pubotibialis and the
puboischiotibialis of the thigh are fused. Fertilization in the
Cryptobranchoidea is external, the cloacal gland complex which
forms the spermatophores of most higher urodeles being reduced
and including only one type of gland. The eggs are always laid
in gelatinous sacs, whether these be short as in the Hynobiidae
or pulled out into two long strings as in the Cryptobranchidae.
The suborder includes only two families, the Hynobiidae, con-
fined to the eastern Asiatic region, and the Cryptobranchidae,
found in eastern Asia (including Japan) and the eastern United
States.

Family 1. Hynobiidae. — The Asiatic land salamanders, often
referred to the Ambystomidae, differ from the latter in retaining
the primitive characters listed above. They represent a very
uniform group both anatomically and in life history. The
family includes five genera. Only one of these, Hynobius, has
an extensive distribution. It ranges from the Urals to Kam-
chatka, Sakhalin, and Islands of Japan and from northern Siberia
to Turkestan and Hupeh. The other four genera occupy very
limited ranges in different parts of the range of Hynobius. They
have apparently arisen directly from some species of Hynobius,
which occur very near their respective ranges. The derived
genera have undergone a number of parallel modifications. This
is, perhaps, the usual mode of generic evolution in the Amphibia.
A widespread stock gives rise to a number of local variants which
differ from the original stock in features which the systematist
considers of generic value. Similar generic characters have
sometimes appeared independently in the divergent branches of
the original stock. In the Salientia, the numerous cases of
parallel evolution are particularly conspicuous (see page 88).

Pachypalaminus is known from only one species taken from a
single locality — Odaigahara Mountain, Yamato, Hondo, Japan.
It agrees closely with Hynobius vandenburghi of the same general
region but differs in having a horny covering to the palms, soles,
and tips of digits. Further, its premaxillary fontanelle is larger.
Batrachuperus, known from two species, is restricted to Szechuan
and to the Thibetan province of Kham. It has redeveloped the

RELATIONSHIPS AND CLASSIFICATION

467

horny pads on the feet found in Pachypalaminus and in addition
has weakened its prevomers in such a way that the vomerine
teeth are restricted to two small widely separated patches,
instead of forming the V-shaped series found in Hynobius and
Pachypalaminus. Ranodon, which includes only one species,
sibiricus, is known only from eastern Semiryechensk and western
Chinese Turkestan but possibly has a greater range. It retains
the unmodified feet of Hynobius but has two vomerine teeth
patches separated as in Batrachuperus. It is a mountain-brook
species and has its lungs partly reduced. In an adult 210 mm.
long these were only 22 mm. in length. The last genus, Onycho-
dactylus, is the most specialized. It ranges from Khabarovka,
Maritime Government, and Wonsan, Korea, to Hondo and
Shikoku. It includes two closely related species, japonicus
and fischeri. These are lungless, like some brook species of
other families. Japonicus is known to frequent mountain
streams, secreting itself under rocks near the water very much as
in the case of the American Dusky Salamander, Desmognathus
fuscus. The vomerine teeth are in a nearly transverse and
continuous series across the palate. The premaxillary fontanelle
is large and the tail, long and nearly cylindrical. The larvae of
Onychodactylus are distinctive, especially in the broad fins on
their limbs (Fig. 53). The digit tips are provided with sharp
recurved claws which are sometimes retained in the adults.
Similar but much smaller claws are found in the larvae of some
species of Hynobius, as, for example, in peropus. The gills of the
larvae have very short rami in correlation with the current in
which they live.

The functional significance of the few characters which dis-
tinguish the genera of Hynobiidae is not clear. Dunn sees in
them adaptations toward a more aquatic life. The habits of
only two genera, Onychodactylus and Ranodon, are known.
These genera frequent mountain brooks but nevertheless lack the
horny pads of the other two genera. The reduction of the
prevomers occurs in terrestrial as well as in aquatic species of
other families. Thus the only characters which can be labeled
as closely correlated with a specific environment are the reduction
of the lungs and certain features of the larvae (short gills, etc.).

It is not only difficult to pick out any highly adaptive characters
in the Hynobiidae, but certain genera exhibit marked differences
which almost surely have no adaptive significance. Perhaps the

468

THE BIOLOGY OF THE AMPHIBIA

most striking of these is the loss of the fifth toe. In Batrachu-
perus this digit is lacking and also in Hynobius keyserlingii, which
is frequently placed in a distinct genus, Salamandrella. The
digit is usually absent in Hynobius kimurai and may occasionally
be missing or absent in other species of Hynobius. In other
families of urodeles the same toe may be lost, and in these its
presence or absence is considered a generic character. But in the
Hynobiidae the toe is so variable in length and its occurrence so
haphazard that the species of Hynobius lacking it cannot be
considered a natural group. Nor is it possible at the present
time to imagine any reasonable functional excuse for its absence
in Batrachuperus.

Family 2. Cryptobranchidae. — The two genera of giant
salamanders which form this family are both semilarval, that is,
incompletely metamorphosed types (Fig. 145) directly evolved
from the hynobiids and exhibiting all the primitive features of the
suborder. Megalobatrachus, found in China and Japan, is less
larval than Cryptobranchus, the Hellbender, of eastern United
States. Gills are lacking in both, but in the adult Megalobatra-
chus the spiracle is closed and only two epibranchials are usually
retained on the essentially larval hyoid. In Cryptobranchus
(Fig. 146) the spiracle remains open, as an outlet for water taken
into the mouth during aquatic buccal respiration, and four
epibranchials are retained. The eyes of both genera are devoid
of eyelids, as is the case in the larvae of all urodeles. Aside
from their giant size and semilarval habitus, the cryptobranchids
may be distinguished from their hynobiid ancestors by various
larval characters of the skull and hyoid, such as the parallel
arrangement of maxillary and prevomerine teeth. The skeleton
has, however, undergone certain specializations of its own. The
whole skeleton is greatly flattened, especially the skull. The
lacrimal and septomaxillary bones have been lost. The crypto-
branchids are completely aquatic animals, and, as they have no
gills when adult, the skin (including the epidermis) has become
greatly vascularized.

Megalobatrachus embraces only a single species, japonicus,
known from China and Japan. Cryptobranchus also includes
only one species. This is widely distributed over eastern United
States from the Great Lakes to Georgia and Louisiana. It is
abundant only in the rivers which flow from the Allegheny high-
land. Megalobatrachus is known as a fossil from the Miocene

RELATIONSHIPS AND CLASSIFICATION

469

of Europe. The closely allied, if not identical, Andrias has been
found in the Miocene and Upper Oligocene of the same region.
A fossil cryptobranchid, Plicognathus, has been described from

Fig. 145. — Diagram illustrating the phylogeny of the urodeles. The heavy-
black arrows indicate the phylogenetic relations. The narrow, horizontal arrows
represent the ontogeny of the various families. The degree of metamorphosis of
the hyobranchial apparatus is employed as the chief criterion of metamorphosis
in this diagram. The "permanent larvae" are not closely related but have been
derived from different groups.

the Lower Pliocene of Nebraska. Hence the family at one time
must have had much greater distribution than now. The crypto-
branchids are river salamanders, japonicus usually frequenting
smaller streams than alleganiensis.

470

THE BIOLOGY OF THE AMPHIBIA

Fig. 146. — Permanent larvae: the perennibranch and derotreme salamanders.
A. Typhlomolge rathbuni. B. Amphiuma means. C. Necturus maculosus. D.
Siren lacertina. E. Cryptobranchus alleganiensis.

RELATIONSHIPS AND CLASSIFICATION

471

SUBORDER 2. AMBYSTOMOIDEA. — The salamanders of the
family Ambystomidae are placed in a distinct suborder, although
they have apparently arisen from hynobiids or from prohynobiids.

Fig. 147. — Some common species of Ambystoma: A. Amby stoma maculatum.
B. Ambystoma jeffersonianum. C. Ambystoma tigrinum. D. Ambystoma opa-
cum. E. Ambystoma texanum.

They possess in common with the Salamandroidea certain ad-
vanced characters such as the fusion of angular to the prearticu-
lar, the loss of the second epibranchial, and the elongation and

472

THE BIOLOGY OF THE AMPHIBIA

approach of the premaxillary spines. Fertilization is internal,
and three sets of glands surround the cloaca of the male. The
Ambystomoidea are distinguished from the Salamandroidea by
their short prevomers without posterior processes extending over
the parasphenoid region. The vertebrae are amphicoelous in
the Ambystomidae and opisthocoelous in the Salamandridae and
some other Salamandroidea. The skull agrees with that of the
Hynobiidae and differs from that of the primitive salamandroids
in lacking a frontosquamosal arch and in retaining, in two genera,
the lacrimal. The hyoid is peculiar in possessing a cartilaginous
cross-bar between the posterior cornua in a large percentage of
the species. The body muscles as far as known are primitive, a

Fig. 148. — Dicamptodon ensatus, a large terrestrial salamander of the west coast
of the United States.

rectus abdominis superficialis but no rectus abdominis profundus
being present.

Family 1. Ambystomidae. — The three American genera
Ambystoma, Dicamptodon, and Rhyacotriton comprise the
family Ambystomidae, which is the only one in the suborder.
Ambystoma includes 11 species widely scattered over North
America from southern Alaska to Mexico. The species are all
much alike in form but differ remarkably in color pattern (Fig.
147). They usually lay their eggs in the water, although the
Marbled Salamander, A. opacum, deposits them on land in the fall.
The larvae, however, are very similar (see page 51) and, being
equipped with broad body and tail fins, are adapted to pond life.

Dicamptodon and Rhyacotriton are both western salamanders.
The latter is apparently restricted to the Olympic Mountains,
Washington, while the former ranges from southern British

RELATIONSHIPS AND CLASSIFICATION

473

Columbia to Southern California. The region they occupy is a
humid coastal belt with moist atmosphere and soil. Both genera
are represented by single species which can be distinguished
from any species of Ambystoma on external characters. Dicamp-
todon is the largest land salamander in the world, attaining a
length of 271 mm. It is heavily marked with blackish brown
(Fig. 148). Rhyacotriton is apparently a dwarf derivative of
Dicamptodon. It is uniform brown above except for a few
white specks. Both genera differ from Ambystoma in possessing
lacrimals. Rhyacotriton differs from Dicamptodon in lacking
nasals. It is a mountain-stream form and has its lungs reduced
to mere vestiges which, although only 5 or 7 mm. long, retain a
circulation and are filled with air. The larvae of Rhyacotriton
and Dicamptodon differ from the Ambystoma species in lacking
a body fin, in having short bushy gills, and in being in other
ways adapted to mountain-stream life (see page 49).

SUBORDER 3. SALAMANDROIDEA. — Any metamorphosed uro-
dele having teeth on the roof of the palate well behind the internal
nares is referable to the Salamandroidea. The prevomers of
the three families in this suborder are either extended back as
two dentigerous processes on each side of the parasphenoid or
split off as one or two groups of teeth patches lying directly on the
latter bone. The Salamandroidea is an extremely varied group
including such aquatic forms as the newt and Amphiuma and
such terrestrial types as the plethodons. It has the widest dis-
tribution of any suborder and seems to have arisen independently
from prohynobiid ancestors not living today. Fertilization is
internal, as in the Ambystomoidea, and three sets of glands
surround the cloaca of the male ; if one is absent it is the outer-
most, the abdominal gland.

Family 1. Salamandridae. — The European Salamandra and
the holarctic newts are grouped together with some less known
forms in the present family. The prevomerine teeth of the group
are distinctive, being carried back as a long, sometimes S-shaped,
row on each side of the parasphenoid. The vertebrae of the
salamandrids are opisthocoelous, while with a few exceptions
those of the genera in the other families of the suborder are
amphicoelous. The primitive salamandrids are large, mostly
rough-skinned newts, having a frontosquamosal arch (Fig. 149),
four-pronged basihyals, high neural spines, and long ribs with
uncinate processes. The more specialized newts have lost the

474

THE BIOLOGY OF THE AMPHIBIA

arches and reduced the hyoid and ribs. The newts lack the
stylus to the columella, while Salamandra and Chioglossa retain
it fused to the periotic. The newts are frequently separated
from the other salamandrids as a distinct family, the Pleurode-
lidae. Since these other genera were apparently derived from
the primitive salamandrids, this arrangement has little in its
favor. Newts retain a primitive body musculature (a rectus
abdominis superficialis, but no profundus), while Salamandra is
specialized in lacking the obliquus internus and in possessing both
rectus muscles. Salamandra is more terrestrial than the newts.

The Salamandridae are Eurasian, except for the American
newts, Triturus. The most primitive salamandrid is Tyloto-

Fig. 149. — Dorsal aspect of the skull of Tylototriton verrucosus showing the
fronto-squamosal arch which characterizes the primitive salamandrids.

triton, represented by two species: verrucosus in Yunnan and the
eastern Himalayas and andersoni of Okinawa Island in the Loo-
choo Archipelago. These are rough-skinned newts, apparently
rather terrestrial in habits. They retain a primitive skull pattern
and the maxillaries extend posteriorly to the squamosals (to
which is apparently fused the quadratojugals). The cartilag-
inous pterygoid of each side is fused to the maxillary, and the
bony pterygoid nearly reaches the same element. A broad
frontosquamosal arch is present and a secondary deposit of bone
is found on various skull elements and on the neural spines.
Pachytriton is apparently a smooth-skinned, aquatic derivative
of Tylototriton. It is known from one species restricted to a
small region in southeastern China. Its bony pterygoids are
broadly attached to the maxillaries, while the latter are broadly

RELATIONSHIPS AND CLASSIFICATION 475

separated from the squamosals. The frontosquamosal arch
of each side is entire but very narrow. The typical newts, Tri-
turus, Pleurodeles, and Euproctus, have apparently been
derived from the same stock as Pachytriton. Some forms (Fig.
150) such as Pleurodeles waltl are rough skinned and resemble
Tylototriton closely. They have specialized, however, in a
reduction of the maxillary and pterygoid elements, a reduction
which is carried farther in the Plethodontidae. In Triturus the
bony pterygoid is small and does not reach the maxillary, and the
latter is short, not reaching the squamosal. In all species of
the genus except T. cristatus, the frontosquamosal arch is either
present or represented by a tough ligament. Triturus, if assumed

Fig. 150. — European salamandrids : A. Euproctus asper. B. Pleurodeles waltl.

to include Pleurodeles and Euproctus, embraces about 24 species
and numerous subspecies. These are scattered over eastern
Asia and Japan, North Africa, Europe, and North America. The
greater number and diversity of species are found in Europe.
Four species are found in North America. The western T.
torosus is a rough-skinned form and may have been derived from
Asiatic species. It is sometimes united with these species in a
separate genus, Notophthalmus. The eastern T. viridescens and
T. dor satis and the southern T. meridionalis seem most closely
related to the European species.

The Italian Salamandrina is merely a European newt lacking
the fifth toe. As emphasized above, this loss has occurred
independently in many different groups of urodeles. Sala-

476

THE BIOLOGY OF THE AMPHIBIA

mandrina includes only a single species, terdigitata. It is a dark,
rough-skinned form with a yellowish or pinkish mark between
the eyes and a brightly marked under surface washed with
salmon or carmine posteriorly.

The smooth-skinned Salamandra and Chioglossa are perhaps
the most terrestrial salamandrids, although the latter genus often
frequents the edges of streams and escapes into the water when
disturbed. They agree with the typical newts in their reduced
pterygoids and maxillaries. They differ from most newts in
lacking the frontosquamosal arch and the pronounced neural
spines. Both Salamandra and Chioglossa may be distinguished
on external characters. Salamandra includes four species scat-
tered over Europe as far east as the Caucasus. They all have
squarish heads and some indication of the paratoid glands which
are so characteristic of the common European Salamandra sala-
mandra. Chioglossa includes a single slim-bodied species,
lusitanica, inhabiting Spain and Portugal. Its most distinctive
feature is a long protractile tongue free on all sides except for a
median partition in front.

Fossil salamandrids have been found in the Oligocene, Miocene,
and more recent formations of Europe. Most of these fossils
are too fragmentary to establish definitely their relationship with
living genera. Tylototriton, living today in southeastern Asia
and one of the Loo-choo Islands, has been recently discovered
in the Miocene of Switzerland. Possibly the fossil described as
Heliarchon was the larva of some species of Tylototriton. Chelo-
triton, Heteroclitotriton, and Megalotriton may be related to the
same genus, while Polysemia has more resemblance to Triturus.
The latter genus has been reported from the Miocene and later
formations of Europe. Although the mutual relationships of
these genera are not known, it is certain that salamandrids were
existing in Europe by at least the Oligocene. It is, therefore,
not surprising that Europe is apparently the center of salamandrid
specialization.

Family 2. Amphiumidae. — The large " Congo Eel" or "Con-
ger," Amphiuma, of southeastern United States is a semilarval
type (Fig. 146) derived from the salamandrids and agreeing with
them in most important characters. It possesses lungs, a bony
pterygoid, a posterior process from each prevomer. The pre-
maxillary spines are elongated to separate the nasals, and a
nasolabial groove is lacking. It parallels the plethodontids in

RELATIONSHIPS AND CLASSIFICATION

477

the loss of the ypsiloid apparatus and the fusion of columella and
operculum, the latter remaining attached by a narrow isthmus to
the periotic. It has retained a number of larval characters such
as the lidless eyes, the parallel arrangement of maxillary and
vomerine teeth, the four branchial arches, and the amphicoelous
vertebrae. These larval features have led to a misunderstanding
of its true relationships, for in most texts Amphiuma is grouped
in the same family with Cryptobranchus. Both genera are
partly metamorphosed aquatic types, but they have arisen from
very different stocks and have no close affinity. Amphiuma is
readily distinguished from the latter by its elongated and rounded,
not flattened, body, its salamandroid skull, and its distinctive
hyoid. The first ceratobranchial and epibranchial are not
separated and the second ceratobranchial is absent. Amphiuma
includes two species, both inhabiting southeastern United States
as far west as Louisiana and Missouri.

Family 3. Plethodontidae. — The majority of American uro-
deles are included in the family Plethodontidae. These may be
brook dwelling or terrestrial. The family apparently arose in
America from a salamandrid stock. One genus succeeded in
extending southward to southern South America and another
invaded Europe, where it is represented by two species in the
Mediterranean region. The plethodontids are more specialized
than the salamandrids in their vomerine teeth which are carried
back by processes during ontogeny to lie over the parasphenoid,
as either one or two dentigerous patches. The pterygoid either
fails to ossify, remaining entirely cartilaginous throughout life,
or is represented by a small bony nodule. The Plethodontidae
embrace a very natural series of genera. They are all lungless
and possess a nasolabial groove to assist in freeing the nostril
from water. The latter character serves alone to distinguish any
plethodontid, but without a hand lens the fine groove from nostril
to lip is sometimes difficult to see. Correlated with a loss of
lungs, the ypsiloid apparatus is reduced or absent. The otic
apparatus seems at first distinctive, for the columella and oper-
culum are fused into a single plate (with or without a style) which
is attached by a narrow cartilaginous isthmus to the periotic. It
is, however, probably derived from the type of otic apparatus
found in the larval salamandrid. The body musculature- of the
plethodontids is specialized, resembling that of the terrestrial
salamandrid, Salamandra.

478

THE BIOLOGY OF THE AMPHIBIA

Fig. 151. — Plethodontid salamanders: A. Hydromantes italicus. B. Aneides
lugubris. C. Batrachoseps attenuatus. D. Eurycealucifuga. E. Desmognathus
quadra-maculatus. F. Typhlotriton speJaeus. G. Gyrinophilus porphyriticus.

RELATIONSHIPS AND CLASSIFICATION

479

The evolution of the Plethodontidae has been studied most
critically by Dunn (1926), who has no doubt sketched correctly
the main outlines of the phylogeny of this dominant group of
American salamanders. There are, however, a number of
obscure points in the relationships of the various genera and the
conclusions reached here are not always those accepted by Dunn.

The most primitive genera are Gyrinophilus (Fig. 151) and
Pseudotriton. They are comparatively large mountain-brook or
spring salamanders (4 to 7 inches long), reddish, pink, or salmon
in color, suffused or spotted with a darker tone. They are con-
fined to eastern United States and are the only reddish sala-
manders in this region save the land form of the water newt.
The latter is small, terrestrial, bright vermillion or olive in color,
and has a rough skin. Pseudotriton may be distinguished from
Gyrinophilus by its usually redder skin, rounder face (the canthus
rostralis lacking), and fused premaxillaries. P. ruber is the com-
mon, red stream salamander of the Appalachians from New
York to the Carolinas.

Eurycea, which is represented by eight species in eastern United
States, is very closely allied to Pseudotriton. It has the free
mushroom tongue of that genus and the complete set of pletho-
dontid skull elements. It is less specialized, however, than
Gyrinophilus in a number of features. Its nasals do not overlap
the premaxillary spines as in that genus, and its periotics and
squamosals are not raised into sharp crests. If we are to assume
that Eurycea was derived directly from Pseudotriton we must
postulate a despecialization in phylogeny, a reversal of evolution.
This is not difficult where the derived structure is a more juvenile
condition, for a mere slowing up of the growth processes would
give the desired result (see page 100). It is probable, however,
that Eurycea was not directly derived from Pseudotriton but
from some more thoroughly mountain-brook type, for it is less
specialized in certain features not only of its skull but also of its
anatomy, as, for example, its skin vascularization (Noble, 1925).

Manculus is a dwarf form of Eurycea ranging from the Caro-
linas to Texas. In color and body form it is almost identical with
the juvenile Eurycea bislineata cirrigera of part of this region.
It differs chiefly in the loss of the fifth (outer) toe. Manculus is
apparently more terrestrial than most races of Eurycea bislineata.

Three highly specialized genera of plethodontids are of uncer-
tain affinities, but they apparently diverged from the more

480

THE BIOLOGY OF THE AMPHIBIA

generalized plethodontid stock represented today by the four
genera just discussed. Stereochilus of the coastal plains of the
Carolinas, Virginia, and Georgia is an aquatic form which retains
the lateral-line organs on the head throughout life. These give
the head a pitted appearance. Stereochilus is primitive (or
juvenile) in retaining the parasphenoid teeth patches continuous
with the vomerine series. It is specialized in having the pre-
maxillary spines almost completely fused together (an aquatic
adaptation correlated with the reduction of the premaxillary
gland). Stereochilus is a small, drab-colored urodele easily
recognized by its pitted head. Typhlotriton of the caves of
Missouri and Arkansas has specialized in another direction. It
is a blind salamander when adult and the only blind urodele which
metamorphoses. The skin is only slightly pigmented, and the
lids, which are visible in the adult, are drawn together (Fig. 151F).
Typhlotriton agrees with Gyrinophilus and Stereochilus in its
continuous vomero-parasphenoid series of teeth. Typhlomolge
of the caves of Texas is a permanent larva which is completely
blind (unlike the larvae of other blind salamanders). It is
specialized in a nearly complete loss of skin pigment and in an
elongation of its slim legs (Fig. 146). It was possibly derived
from Typhlotriton, for it agrees closely with the larva of Eurycea
and other primitive plethodontids. Stereochilus, Typhlotriton,
and Typhlomolge are each known from only a single species
which, because of its peculiar habits and habitat requirements,
is very local.

A second group of genera, apparently derived from Eurycea or
its allies but not showing in their anatomy a very close relation-
ship to them, is formed by the dusky salamanders, Desmogna-
thus and Leurognathus. The first of these two genera includes
the commonest salamanders of eastern United States. They
both have the tongue attached in front. Dunn considers this a
primitive character, but as the late larva of Eurycea has an
attached tongue it might equally well be considered a juvenile
character. Desmognathus and Leurognathus are unquestionably
specialized in the lost (or fused) prefrontals and in the modified
occipital condyles, atlas, and temporal muscles which function
in preventing the lower jaw from opening more than a third the
usual gape (see above, page 264), the remainder of the opening
being accomplished by raising the skull on the atlas. Leurogna-
thus has been derived directly from Desmognathus quadramacula-

RELATIONSHIPS AND CLASSIFICATION 481

tus. It agrees very closely with this species in color pattern and
form, but its head appears a trifle more depressed. An examina-
tion of its skull, however, reveals that a number of pronounced
internal changes have occurred. The vomerine teeth are reduced
or lost. The skull is flattened and the internal nares shifted
laterally (Fig. 44). The premaxillary fontanelle is closed. The
functional significance of the loss of teeth and flattening of the
skull is not clear, but the reduction of the pre-
maxillary fontanelle is probably correlated with
a degeneration of the premaxillary gland, which
could be of little use to aquatic forms, as they
have no need of moistening their tongue with
a sticky secretion. Leurognathus embraces two
races confined to North Carolina, where Des-
mognathus quadramaculatus is most abundant.
It is more aquatic than any species of Des-
mognathus. The latter genus includes seven
forms extending from eastern Canada to Kan-
sas. Most frequent the vicinity of mountain
streams, but the small D. fuscus carolinensis
and D. f. ochrophaeus have rounder tails and are
more terrestrial than the others. The larvae
(Fig. 152) may be distinguished from those of
Eurycea in the same streams by their shorter,
brushlike gills.

A third group of Plethodontidae includes
Plethodon and its close allies. These are all Fig. 15 2. — A
terrestrial species, laying their eggs on land and, 1frva °f Desmogna-

* ... ' thus phoca showing

except for one genus, passing their entire life away the brush-like gills
from the water. Plethodon seems to be the cen- characteristic of the
tral group of this series. It has free premaxillae
and a tongue attached in front but is otherwise essentially like
Eurycea. Plethodon includes 11 species distributed over almost
the entire United States and southern Canada. Hemidactylium,
the four-toed salamander of the eastern United States, is a
dwarf form of Plethodon which parallels to a certain extent Man-
culus, the dwarf form of Eurycea. Its outer toe has been lost. It
also differs from Plethodon in the basal constriction of the tail, a
provision for quick autotomy. Hemidactylium scutatum, the
only species in the genus, may be readily distinguished from any
species of Plethodon by its pale ventral surface spotted with

482

THE BIOLOGY OF THE AMPHIBIA

large, black blotches. Hemidactylium ranges as far south as the
Gulf states and as far west as Michigan and Arkansas.

Batrachoseps, the Worm Salamander, has been derived from
Plethodon in the west and, like Hemidactylium, has lost the
outer toe. It is much more specialized than that genus in its
elongate body (Fig. 151, C). Its premaxillae are fused and it
has lost the prefrontals. Ensatina is another western derivative
of Plethodon and differs from this genus only in having a basal
constriction of the tail and in possessing certain tubercles on the
palm. Aneides, the last genus in this group, may have arisen
from Plethodon in the east, for its least specialized species is
found in West Virginia, Tennessee, and the Carolinas. Aneides
is the most specialized of all these genera in its fused premaxillary
spines, elongated maxillary and mandibular teeth, and bent
maxillary bone free of teeth posteriorly. It also has Y-shaped
terminal phalanges unlike any of the other genera in the group.

The last group of genera in the family is characterized, as far
as known, by ovo viviparity. Dunn (1926, page 31) assumes that
the genera arose from some terrestrial stock but makes no attempt
to trace their ancestry among the known terrestrial plethodontids.
Hydromantes seems closely related to Oedipus, as evinced by
partly webbed digits (Fig. 151, A), the large nostrils in the young,
the color pattern, and the weakening of the premaxillary spines.
Some species of Oedipus have lost the prefrontals and septomaxil-
las, as in Hydromantes, and a few species have a non-constricted
tail, as in that genus. Both Oedipus and Hydromantes have
boletoid tongues and long epibranchials to support a long tongue.
Lastly they are the only plethodontid genera with different species
in two continents, which speaks well for their traveling ability.
The only character which separates Hydromantes from all
species of Oedipus is its unfused premaxillaries. In view of the
known variability of this bone in a related genus (Eurycea), it
does not seem necessary to hypothecate a separate ancestry for
Hydromantes.

Oedipus includes 30 or more species spread over the neotropics.
Except for three ambystomas in Mexico, the genus includes all
the neotropical urodeles. Some species have broad, padlike feet
with the digits hardly visible. Other species, usually referred to
Oedipina, have very long bodies and short legs. This is a modi-
fication parallel to that of Batrachoseps and suggests common
ancestry of the genera. Hydromantes is known from only three

RELATIONSHIPS AND CLASSIFICATION

483

species: one the rare Yosemite Salamander, H. platycephalus,
and the other two commonly combined under the name, Spelerpes
fuscus. This name embraces two closely related forms: H. genei
of Sardinia and H. italicus of the French Alps and part of Italy.

It has been assumed on the basis of life history that Oedipus
and Hydromantes have arisen from Plethodon. The chief objec-
tion to this view is the occurrence of a free boletoid tongue in
these genera and an attached tongue in Plethodon. It should
also be considered that Plethodon has a broad distribution, while
Eurycea, with which Oedipus agrees most closely in adult struc-
ture, has a restricted range in eastern United States. Thus, in
reaching a conclusion in regard to the probable ancestry of
Oedipus, we must weigh all its obvious terrestrial characters
against its boletoid tongue. With the available data no final
conclusion can be reached at this time.

SUBORDER 4. PROTEIDA.— The Mud Puppy, Necturus, and
the European Blind Salamander, Proteus, form a natural group
of permanently larval salamanders of unknown ancestry. They
are placed in a distinct suborder, as their relationship to any of
the other primary groups of urodeles is uncertain. They have
no relationship to Spelerpes or to the Plethodontidae, as some-
times stated. Lungs are present but the ypsiloid apparatus is
absent. They are, therefore, bottom walkers. The pubois-
chium is distinctive. It is large and pointed anteriorly. Colu-
mella and operculum are fused together and are free from the
periotic. The more obvious characters of the Proteida are all
larval features found in the larvae of other families. The skull is
largely cartilaginous, the maxillae are absent. Palatines and
pterygoids form a continuous series. Eyelids are lacking, and
long external gills are retained. The branchial apparatus is
larval, but the fourth branchial arch is lost. The body muscles
are larval in that the rectus abdominis is lacking. The Proteida
may have originated from some salamandroid, for they possess
the usual cloacal glands of that group and practice internal
fertilization. Further the premaxillary spines are long in both
genera, and the angular and prearticular are fused.

Family 1. Proteidae. — The European "Olm," Proteus, with
its long, pigmentless body and its "very larval" appendages
provided with only three fingers and two toes cannot be confused
with other permanent larvae, nor can Necturus with its external
gills and pigmented body. The internal characters which define

484

THE BIOLOGY OF THE AMPHIBIA

the Proteidae are the same as those of the suborder. Necturus,
the well-known Mud Puppy of zoological laboratories, is repre-
sented by only two species and one subspecies. N. punctatus is
found chiefly in the lower courses of the rivers of North and
South Carolina, but it manages to reach the Piedmont of North
Carolina. It is a small, uniformly colored species and probably
represents a dwarf derivative of N. maculosus confined to the
Carolina coastal plain. The other Carolina Necturus resembles
closely maculosus, the common Mud Puppy of eastern United
States, but fails to reach the size of this species. It has, therefore,
been considered a distinct subspecies, N. maculosus lewisi. The
typical form, N. m. maculosus, ranges from the Great Lakes to
Louisiana and east to the Atlantic.

SUBORDER 5. MEANTES. — The sirens are permanent larvae
which have developed a few adult characters. They agree with
the very young larvae of other families in possessing only the
anterior appendages. Their relationships are uncertain. It is
possible they were derived from some hynobiid, for the premaxil-
lary spines are small and the nasals meet. No cloacal glands are
present in either sex, and hence fertilization is very probably exter-
nal. Both jaws are covered with horn, unlike those of all other
urodeles save certain larval hynobiids and ambystomids which
have a horny predentary sheath. They differ from larval
hynobiids in the greatly elongated body, the fused angular and pre-
articular, and the distinctive skull form. It is frequently claimed
that the Meantes are adults which have "reverted" to an aquatic
habitat. The chief characters used to support this claim are the
separate prevomers and pterygoids, the separate ossification of
the coracoid, and the specialized Jacobson's organ. The latter
two features are peculiar to the Meantes, while the first appears
when the rest of the animal is a typical larva in structure (see
page 102). The usual characters of a young larva are found in
the adult sirens, namely lidless eyes, three pairs of external gills,
and lacking maxillaries. The skin of Siren, unlike that of
Pseudobranchus, is that of a typical land salamander. As
stated before (page 103), the skin alone of all the structures of the
juvenile Siren undergoes a typical metamorphosis.

Family 1. Sirenidae. — The two genera included in the Sireni-
dae may be readily distinguished from all other permanent larvae
by their possessing only the anterior appendages. Pseudo-
branchus is much smaller than Siren and is striped with brown

RELATIONSHIPS AND CLASSIFICATION

485

and yellow on the body and is not uniform slate, like the half-grown
Siren. It is a slimmer form than Siren and possesses only one
branchial opening. Pseudobranchus, unlike Siren, is a burrow-
ing salamander and when confined in aquaria readily burrows out
of sight if the sandy floor is suitable. Siren, however, frequently
works its way through the densely matted vegetation bordering
its native ponds. Hence, the habits of the two genera are not
sharply distinguished.

ORDER 6. SALIENTIA. — The frogs and toads form a natural
group of Amphibia characterized by short, tailless bodies and
long legs. The posterior limbs have four segments, not three as
the salamanders, and these function as powerful levers, permitting
most Salientia to make long leaps.

The frogs and toads are included in a single order, Salientia.
Various names are in general use for the group : " Anura," " Batra-
chia Ecaudata," and "Batrachia," but the name used here has
been adopted by most systematists.

Unfortunately the fossil record does not help in elucidating the
evolution of the various suborders or families of Salientia. The
oldest known fossils are Montsechobatrachus from the Upper
Jurassic of Spain and Eobatrachus from the Upper Jurassic of
Wyoming. The systematic position of neither genus has been
definitely established, but since both exhibit the general propor-
tions of the frogs and toads, it is obvious that the Salientia
have possessed their characteristic body form since at least the
Jurassic.

SUBORDER 1. Amphicoela.— The most primitive Salientia
living today are included in the Amphicoela. They are distin-
guished from other frogs by their amphicoelous vertebrae, the
interdorsal and interventral remaining cartilaginous as in the
majority of urodeles. The suborder includes only a single
family.

Family 1. Liopelmidae. — There are only two genera of
Amphicoela and these are included in a single family, although
one genus is found only in New Zealand and the other only in
northwestern United States. Both genera are more primitive
than other Salientia (Fig. 153) in possessing two tail-wagging
muscles, the pyriformis and the caudalipuboischiotibialis, even
though neither possesses a tail. Liopelma and Ascaphus are
both small, grayish frogs sometimes suffused with pinks, browns,
and yellows. Ascaphus is the only frog which possesses an

486

THE BIOLOGY OF THE AMPHIBIA

extension of the cloaca in the male (Fig. 154). This is used in
copulation, fertilization being internal in this genus.

SUBORDER 2. OpisTHOCOELA.— The Discoglossidae and
Pipidae are unquestionably closely related. They are the only
Salientia which exhibit typical opisthocoelous vertebrae, -with
well-fused centra (Fig. 155). Their scapulae are shorter than
in the other Salientia, even though some forms may be terrestrial
and others aquatic. The Opisthocoela are also primitive in
possessing free ribs either in the larva or in the adult. Their

Fig. 153. — Diagram illustrating the phylogeny of the Salientia.

muscular system approaches closely that of the Liopelmidae. On
the other hand, some pipids have the most specialized skulls and
sacra of all Salientia, and some discoglossids have the most
advanced urogenital system. The tongueless condition of the
Pipidae is an extreme aquatic specialization almost paralleled by
the tongue reduction in the thoroughly aquatic species of Batra-
chophrynus, a bufonid.

Family 1. Discoglossidae. — The Discoglossidae are far less
specialized than the Pipidae, although some, such as Bombina,
spend most of their time in the water. They may be described
as Opisthocoela with a fully arciferal pectoral girdle, ribs pres-

RELATIONSHIPS AND CLASSIFICATION

487

ent in the adult, sacral vertebra free with biconvex centrum,
presacral vertebrae not less than eight, tongue and eyelids
present. The Discoglossidae include only two European,
one Eurasian, and one Philippine genus. These may be readily
distinguished by their external form, the European species being

b c

Fig. 154. — Male Ascaphus truei: A. Showing the cloacal appendage of this sex.
B. The appendage viewed ventrally. C. The same fully distended, showing the
spines which occur within the orifice of the cloaca.

well known. Bombina includes four species of depressed
water toads, all variegated below, with black and some other
tone, either white, red, or orange. Two of the species are
European and two Chinese. Discoglossus includes only a single
species, pictus, from southwestern Europe and northwestern
Africa. It is a Rana-like frog, about the size of a Pond Frog,
R. clarnitans, and grayish in color, often with a pleasing pattern of

488

THE BIOLOGY OF THE AMPHIBIA

Fig. 155. — The principal types of vertebral columns of the Salientia: J..
Amphicoelous — Ascaphus truei. B. Opisthocoelous — Alytes obstetricans. C.
Opisthocoelous with fused coccyx — Xenopus tropicalis. D. Anomocoelous —
Scaphiopus couchii. E. Procoelous — Atelopus varius. F. Diplasiocoelous —
Rana virgatipes. The vertebral columns are viewed from the ventral aspect.

RELATIONSHIPS AND CLASSIFICATION

489

darker and lighter tones. Alytes is a smaller, more terrestrial,
and rougher-skinned form. It is usually lighter in coloration.
Alytes is represented by two species: one, obstetricans, is widely
spread over western Europe, and the other, cisternasii, is restricted
to Spain and Portugal. Barbourula, recently described from the
Philippines, is a completely aquatic frog known from one Philip-
pine species which resembles Ooeidozyga closely. Its most dis-
tinguishing feature is its webbed fingers.

Fossil discoglossids are known from the Upper Oligocene and
Miocene of Europe. Latonia of the Upper Miocene of Switzer-
land shows some affinity to Discoglossus but differs in certain
characters of its skull and in the larger size. The affinities of
Pelophilus and Protopelobates are less certain. Alytes has been
described from the Lower Miocene of Bonn. Although these
few fossils give no picture of the origin or evolution of the Disco-
glossidae, it is obvious that the family was established in Europe
by at least the Middle Tertiary.

Family 2. Pipidae. — The Aglossal Toads are purely aquatic
Salientia. In correlation with this habitat they have lost a
tongue and movable eyelids (except Pseudhymenochirus, which
retains lower eyelids). Ribs are free in the larva but ankylose
to the diapophyses on metamorphosis. Various fusions occur in
the vertebral column, the presacral vertebrae numbering five to
eight. The sacrum is fused to the coccyx (rarely free and with
a single condyle). The pectoral girdle is partly or wholly firmis-
ternal; the cartilages never broadly overlap as in the Discoglos-
sidae. The African pipids differ strikingly from the South
American genera (Fig. 156) in appearance and life history. They
may be conveniently placed in different subfamilies. In each sub-
family the most primitive genus possesses maxillary teeth and
the more specialized ones lack these structures entirely. The
Pipidae are found only in Africa and South America.

Sub-family 1. Xenopinae. — Pipids with simple pointed digits,
the three inner toes tipped with black, horny claws; eggs, as
far as known, small; the tadpole with two long tentacles and a
right and left spiracular opening. The Xenopinae are African,
and include three genera: Xenopus, Hymenochirus, and
Pseudhymenochirus.

Xenopus has the widest distribution and is the most primitive.
Its pectoral girdle is only partially firmisternal. The pterygoids
of each side do not fuse together around the median opening of

490

THE BIOLOGY OF THE AMPHIBIA

the Eustachian tubes, as in Hymenochirus. The prevomers are
present in X. laevis and X. clivii, although fused together. The
skull of even the most primitive species is, however, very special-
ized, especially in the fusion of the sphenethmoid and para-
sphenoid (which form a bony case for the brain), the reduced
and forwardly extended squamosal, the reduced maxillae, and
the peculiar Eustachian tube passage. Xenopus is represented
by five living species.

Hymenochirus is known from three or four species from the
rain-forest and lower Congo. It is the most specialized of all
Pipidae in several features of the skeleton. The pterygoids and

Fig. 156. — Pipid toads: A. Xenopus mi'dleri. B. Pipa pipa, female with eggs.

exoccipitals are fused to form a complete cover to the Eustachian
tubes, which open into the pharynx through a single median
orifice. The lateral wall of the brain case is completely ossified.
The sacrum consists of the VII, VIII, and IX vertebrae fused
together and to the coccyx. All the vertebrae are irregularly
sculptured, and in one skeleton examined, the IV vertebra was
biconvex. The I and II vertebrae are normally fused, which
leaves only five presacral segments. The most remarkable
features are the bladelike flanges of bone which appear on the
ilium, femur, tibia, fibula, tarsals, and metatarsals. These are
widest on the two outermost metatarsals (fourth and fifth).
There are three flanges to each bone and they face in three direc-
tions. No flanges appear on the forelimbs. The pectoral girdle
is completely firmisternal.

RELATIONSHIPS AND CLASSIFICATION 491

It is said that Hymenochirus shows affinity to Pipa. Aside
from its lack of maxillary teeth there are a number of other
resemblances. The most important seems to be the broad and
laterally flanged frontoparietals, the large nasals, the greatly
reduced squamosal, the overlapping, not laterally turned-up,
zygapophyses, the flanging of the leg bones, and the synsacrum.
It is, however, much more specialized than Pipa in its skull,
sacrum, and leg bones. It would seem as easy to derive Hymeno-
chirus from Xenopus as from Pipa. Further, the recently dis-
covered Pseudhymenochirus seems an exact intermediate in
external characters between Xenopus and Hymenochirus. Our
knowledge of the skeleton of Pseudhymenochirus is so fragmen-
tary that no detailed comparison can be made. It is known
from only a single specimen found to the north of the African rain
forest.

Subfamily 2. Pipinae. — Pipids with a starlike cluster of dermal
appendages at the ends of their fingers, eggs carried in individual
dermal pockets on the back of the female, the young escaping
fully metamorphosed. The Pipinae include two closely allied
genera from the Amazonian and northern parts of South America
(including Trinidad). Protopipa is the less specialized in body
form. It retains the maxillary teeth, while Pipa lacks them.
Pipa includes three species differing in body size and egg size.
P. pipa is the largest species and is also the flattest, with dermal
flaps at the angles of the jaws and a filament at the premaxillary
symphysis. The jaw flaps are reduced in P. snethlageae, the head
is smaller, and the premaxillary filament is lacking. P. snethlageae
does not reach the size of P. pipa. The smallest species is P.
parva, which lacks the head ornaments entirely. P. snethlageae
and Protopipa have the fewest number of eggs, but to judge from
the embryos these are larger than in the other species and they are
confined to only the median area of the parent's back.

SUBORDER 3. AnomocoeLA.— The pelobatid toads in their
skeleton and musculature form an intermediate group between
the two preceding suborders and the bufonids. They do not
merge into the latter, as is often stated, but form a rather uniform
group of genera showing no close affinity to any living bufonids.
The Pelobatidae are referred to a distinct suborder, the Anomo-
coela, which may be defined as follows: Salientia without free
ossified ribs at any stage of development; sacral vertebrae pro-
coelous, ankylosed to coccyx or, if free, with only a single artic-

492

THE BIOLOGY OF THE AMPHIBIA

ular condyle for the latter; presacral vertebrae eight, either
uniformly procoelous or with free intervertebral discs.

Family 1. Pelobatidae. — Pelobatids may be either toad- or
froglike in external appearance. They agree with bufoninae in
their arciferal pectoral girdle and dilated sacral diapophyses.
They differ from them in their single coccygeal condyle and
primitive pectoral and thigh musculature (the latter specialized
in the Sooglossinae) . The supracoracoideus muscle is not dif-
ferentiated into an episterno-cleido-humeralis longus and a supra-
coracoideus profundus. The sartorius and semitendinosus form a
single muscle exposed on the ventral surface of the thigh. The
Pelobatidae are distributed across the northern hemisphere from
Mexico and the United States to southeastern Asia and the
Philippines. They penetrate into the southern hemisphere in
the East Indian region, where they occupy the western part of
the Indo-Australian Archipelago but do not reach New Guinea
or the Aru Islands. Further, one subfamily, the Sooglossinae, are
restricted to the Seychelle Islands. The Pelobatidae are known
from three natural groups of genera: the Megophryinae, Pelo-
batinae, and Sooglossinae.

Subfamily 1. Megophryinae. — Pelobatidae with free inter-
vertebral discs (interdorsals) or at least these discs more or less
exposed. Most species of the Megophryinae have their discs
free. Their vertebrae thus approach the embolomerous type of
the first tetrapods. This, however, is a purely secondary modifi-
cation, but one found elsewhere among the Salientia only in the
Criniinae. The vertebrae of the Megophryinae are more
advanced than those of the Criniinae in that the notochord is
replaced by calcification or ossification. In some species of
Megophrys, better known as Megalophrys, the intervertebral
discs may become more or less firmly attached to the vertebrae
immediately anterior to them. The vertebral column in these
specimens is procoelous, as in the Pelobatinae, and the vertebrae
differ from those of the latter only in the extent to which the
intervertebral discs are exposed. The Megophryinae embrace a
group of Asiatic and East Indian pelobatids, some of large size
and striking appearance (Fig. 157B).

The most primitive genus in the subfamily is the widespread
Megophrys or Megalophrys (including Leptobrachium). It is
represented by 25 species distributed across southern Asia and
the western end of the Indo-Australian Archipelago. In Megalo-

RELATIONSHIPS AND CLASSIFICATION

493

phrys the pupil is vertical; the maxillary teeth are well developed,
but the vomerine may be more or less reduced or absent; the
omosternum is cartilaginous or calcified; while the sternum has a
long, bony style. Nesobia of the Natuna Islands is a Megalo-
phrys with a horizontal pupil. Scutiger of the Himalayas is a
rough-skinned, high-mountain Megalophrys with short maxillary
teeth. Aelurophryne of the same region is a Scutiger which has
carried the specialization farther and lost the maxillary teeth
entirely. Ophryophryne, from the mountains of northern
India, is a small-headed Megalophrys without teeth and with a
horizontal pupil. The Bornean Leptobrachella is a diminutive
Megalophrys with a cartilaginous sternum. Leptobrachella,

Fig. 157. — Pelobatid toads: A. Sooglossus sechellensis. B. Megophrys nasuta.

Ophryophryne, and Nesobia, are each known only from a single
species. Scutiger is represented by two closely related species
and the same may be said for Aelurophryne. Thus it is highly
probable that all these genera are merely local specializations of
the Megalophrys stock in comparatively recent times and not
groups which have given rise to any of the higher Salientia, as
some herpetologists have maintained.

Subfamily 2. Pelobatinae. — Pelobatids with the presacral
vertebrae uniformly procoelus, sacrum fused to the coccyx,
except in Pelodytes, which has a single condyle. The American
Scaphiopus and the European Pelobates are popularly known as
the "Spade-foot Toads," because of the broad, sharp-edged tuber-
cle which they carry on the inner side of the foot. The bony core
of this tubercle is formed by the prehallux greatly enlarged as an

494

THE BIOLOGY OF THE AMPHIBIA

instrument for digging. Spade-foot Toads with their vertical
pupil and smooth or slightly tubercular skins (Fig. 158) may be
readily distinguished from the true toads, Bufo, which have a
horizontal pupil and rough skin. Pelodytes, the third genus in
the subfamily, lacks the " spade" of the other genera and is much
slenderer and more froglike. It is known from two species, one
in southwestern Europe and the other in the Caucasus.

The Pelobatinae are closely allied. Scaphiopus with its
cartilaginous sternum seems more primitive than either Pelo-
bates or Pelodytes, which have bony sternums. On the other
hand, Pelodytes with its free coccyx and Rana-like habitus seems
less specialized than either Pelobates or Scaphiopus. The three
genera are obviously closely allied (Boulenger, 1899; Noble, 1924),
although it is difficult to state which stands nearest the ancestral
stock from which they sprang.

Fig. 158. — The eastern Spade-foot Toad, Scaphiopus holbrookii.

The history of the Pelobatinae dates back to at least the Oli-
gocene. Macropelobates is known from the Oligocene of Mon-
golia. Pelobates and a closely allied genus have been described
from the Lower Miocene of Europe. Other fossils, possibly
identical with living species of Pelobates, have been reported
from the Pleistocene of Germany. In brief, Spade-foot Toads
were established in the Old World for the greater part of the
Tertiary.

Subfamily 3. Sooglossinae. — Pelobatids with a free coccyx, a
horizontal pupil, and a ranid type of thigh musculature (the
semitendinosus is separate from the sartorius and lies deep within
the thigh musculature; its distal tendon passes dorsal to that of
the gracilis major and minor). The three Seychelle Island frogs,
Nesomantis thomasseti, Sooglossus sechellensis, and S. gardineri,
have recently been shown to be pelobatids (Noble, 1926), although
the first two have the external appearance of the ranid Arthro-
leptis and the last of the bufonid Nectophrynoides. Sooglossus

RELATIONSHIPS AND CLASSIFICATION

495

(Fig. 157A) is merely a Nesomantis without vomerine teeth, but
gardineri has succeeded in developing short webs between both
fingers and toes while retaining the body form of sechellensis.
Sooglossus lays its eggs on land and the larvae which are devoid
of both internal gills and spiracle adhere to the back of the male.

SUBORDER 4. PROCOELA. — The true toads, tree toads, and
brachycephalid toads form a very natural group of families
characterized by a uniformly procoelous vertebral column and a
double condyle to the coccyx. Very rarely, the latter is fused
to the sacrum, but usually it is free and serves to distinguish the
Procoela from the Anomocoela, or Pelobatidae. The presacral
vertebrae are five to eight in number and lack ribs. The thigh
musculature also is distinctive. The semitendinosus is separate
from the sartorius (Fig. 96) and is more or less covered by the
gracilis and adductor mass. Its tendon joins that of the sartorius
and is ventral to (rarely pierces) the gracilis major and minor.
The Procoela includes one extinct family, Palaeobatrachidae, and
three recent ones, Bufonidae, Brachycephalidae, and Hylidae.

Family 1. Palaeobatrachidae. — The fossil toads of the genus
Palaeobatrachus, and possibly Protopelobates, are grouped
together in the family Palaeobatrachidae. They differ from the
Pelobatidae in having a double condyle on the coccyx and in
having the sacrum formed of two or three slightly dilated pre-
coccygeal vertebrae. They are procoelous and cannot be con-
fused with the Pipidae, which they seem to parallel in several
respects, chiefly in the form of their appendages. In Palaeo-
batrachus luedecki, for example, the metacarpals are as long as
the radius and only slightly shorter than the humerus. This
suggests an aquatic life. The Palaeobatrachidae are sometimes
described as Aglossa or at least as very primitive. Some species,
possibly all, possessed maxillary and vomerine teeth. But aside
from this they possessed few primitive characters. The first and
second vertebrae were probably fused. The others were pro-
coelous without a trace of the notochord (luedecki). Neither
pectoral nor pelvic girdle approached closely to those of the
obviously primitive Liopelmidae. The Palaeobatrachidae extend
from the Jurassic (Vidal, 1902) to Miocene. They are known
only from European formations.

It is not improbable that a number of different stocks are
included under the name " Palaeobatrachus." Thus, in the
Lower Miocene beds near Markersdorff, Czechoslovakia, there were

496

THE BIOLOGY OF THE AMPHIBIA

found many skeletons of Palaeobatrachus luedecki and also some
large tadpole skeletons attributed to the same species. These
tadpoles have single frontoparietal plates similar to those of the
adult skeletons. They also have long parasphenoids extending
forward to a sharp point. In these features they resemble the
tadpoles of Xenopus. In the Rott beds near Bonn, there is
another type of tadpole attributed to Palaeobatrachus diluvianus.
This has a much smaller head, separate frontoparietals, and a
shorter parasphenoid. It seems hardly likely that these two
tadpoles are referable to the same genus.

Family 2. Bufonidae. — The toads, including those with and
those without maxillary teeth, form one of the dominant groups
of Salientia. They resemble the Pelobatidae closely but, as
indicated in the definition of the Procoela, have advanced
beyond this group in both their skeletal anatomy and their
musculature. The toothed bufonids are frequently designated
as Cystignathidae or Leptodactylidae. They are more primitive
than the toothless genera, but as they have given rise to toothless
bufonids in different parts of the world, it makes a more natural
system to group toothed and toothless genera together as a single
family. The Bufonidae possess an arciferal pectoral girdle.
The sacral diapophyses are cylindrical or dilated. The presacral
vertebrae are usually eight, rarely seven. The terminal pha-
langes may be simple or T-shaped. The Bufonidae group them-
selves into seven subfamilies, some better defined than others.

Subfamily 1. Criniinae: Australian Toads. — Bufonidae usually
with a persistent remnant of the notochord continuous throughout
the vertebrae; sacral diapophyses more or less dilated; sternum
broad, cartilaginous, rarely bony; maxillae usually very deep.
The Australian Bufonidae, although represented by 16 genera,
are particularly distinguished by their lack of specialization.
They are all much alike, the characters which separate the genera
being for the most part very trivial. The Criniinae are not
sharply distinguished from the Pseudinae. They differ from most
of the latter by their dilated sacral diapophyses, but unfortunately
a few species of Paludicola, Eupemphix, and Calyptocephalus
have also developed a slightly dilated sacrum. The deep maxillae
serve to distinguish the skulls of most Criniinae. In these the
maxillae are usually more than a fourth as wide as long, while
in the Pseudinae they are much narrower. A few intermediates,
however, exist, and in several species of both subfamilies a second-

RELATIONSHIPS AND CLASSIFICATION 497

ary deposit of bone over the skull elements extends their dimen-
sions considerably. The most fundamental difference would
seem to be the persistent notochord of the Criniinae, but this
character has been checked for only a limited number of genera
and was found to be lacking in one of these, namely Lechriodus.
It must be admitted that until the anatomy of the Australian
and South American bufonids has been more fully investigated
no sharp distinction may be made between the Criniinae and
Pseudinae. Among the peculiar osteological features found in
some but not all Criniinae are the fusion of the first and second
vertebrae, the broad extension of the premaxillaries, and the
reduction in size of the squamosals.

Perhaps the most distinctive group of Criniinae are the large,
smooth-skinned genera, with vertical pupils and normal fingers.
Mixophyes is Rana-like with extensively webbed toes, the web
extending between the metatarsals. Lechriodus (including Phan-
erotis, which apparently has the same shaped pupil) has the toes
only slightly webbed. It is confined to New Guinea and the Aru
Islands, not reaching Australia proper.

Ranaster and Limnodynastes are smaller Salientia with a
transverse row of vomerine teeth behind the choanae. In Ranas-
ter, a New Guinean genus, webs are lacking between the toes and
the skin is very warty. Limnodynastes is widely spread over
Australia. Its toes are either free or slightly webbed. It may
be distinguished from Ranaster by its vertical pupil and less
rugose skin.

Helioporus and Philocryphus are large Australian Criniinae
with free fingers and webbed toes. The latter genus differs from
the former only in its distinct tympanum.

One group of Australian genera is characterized by the dispro-
portionate growth of the fingers. The first finger is much longer
than the second and more or less opposed to it. This group
embraces two genera, Chiroleptes and Mitrolysis. Chiroleptes
(including Phractops) embraces species with the appearance of
Pseudis and others resembling Ceratophrys. Thus it is probable
that the species have very different habits while retaining the
distinctive " opposable thumb" of the group. Mitrolysis is a
Chiroleptes with a vertical pupil.

The greatest number of Criniinae are small Salientia, without
webs between fingers or toes. The metatarsals in these are
bound together. The omosternum and sternum are present and

498

THE BIOLOGY OF THE AMPHIBIA

cartilaginous, as in most Criniinae. The central type is Crinia.
Pseudophryne is identical with it except in lacking maxillary
teeth. Hyperolia may be described as a Crinia with a vertical
pupil. Adelotus and Philoria have the horizontal pupil of Crinia.
They are said to differ from Crinia only in their larger sternum.
Cryptotis is apparently very similar to the same genus but is
said to have a rudimentary omosternum. Cryptotis brevis is
remarkable for a long tusk-like process on the dentary. An exact
analysis of the mutual relationships of these genera will have to
await a more complete knowledge of their anatomy.

The most aberrant Criniinae are the grotesque, fossorial
Myobatrachus and Notaden. Both lack maxillary teeth and
have the sternum more or less calcified or bony. Myobatrachus
has a smooth palate, while that of Notaden is covered with a
series of three soft folds. The immediate ancestors of these
peculiar forms are not living in Australia today, but it is a fair
assumption that they were toothed forms and not so aberrant
as these genera. Neither Myobatrachus nor Notaden shows in
their internal anatomy a close affinity to bufonids found today
outside Australia. They are not Bufoninae, as often stated.

The Criniinae are structurally the most primitive bufonids.
They apparently left no fossil record except in India, when during
the Eocene a little frog closely allied to Crinia lived in consider-
able numbers. This frog has recently been described under the
name of "Indobatrachus." It previously masqueraded under
the name of "Rana" and "Oxyglossus," but even today its skele-
ton is not completely known.

Subfamily 2. Heleophryninae. — Bufonidae with solid procoe-
lous vertebrae, T-shaped terminal phalanges, and a distinctive
thigh musculature; the semitendinosus superficial as in the Pelo-
batidae but separated from the sartorius distally. The only
genus of Bufonidae with maxillary teeth in Africa is sufficiently
distinct from the toothless forms on the same continent or from
the bufonids on other continents to warrant its separation as a
separate subfamily. Heleophryne is now known from five species,
all from South Africa. They have the appearance of slim-bodied
tree frogs or broad-disced species of Lechriodus. The tadpoles
of three species are known. These are all highly modified for life
in mountain streams. The very recent discoveries of de Villiers
and his students indicate that two genera, one of them firmister-
nal, may have been confused under the name Heleophryne.

RELATIONSHIPS AND CLASSIFICATION

499

Subfamily 3. Pseudinae: South American Frogs. — Bufonidae
with solid procoelous vertebrae, cylindrical or rarely slightly
dilated sacral diapophyses, a cartilaginous omosternum and
sternum (the latter sometimes calcified), and with maxillary teeth
usually present. The Pseudinae represent the most primitive
stock of neotropical bufonids. They are confined to South and
Central America and the West Indies, except for a few stragglers
which reach Texas and Florida. One genus, Eleutherodactylus,
is represented by numerous species which form a large part of
the Amphibian fauna of Central America and the West Indies.
The Pseudinae, although not sharply distinguished from the
Criniinae, cannot be confused with other neotropical bufonids
because of their girdles. The sternum is broad and cartilaginous
except in large specimens of Calyptocephalus, Ceratophrys, and
Hylorina, where it may calcify. Bufo has a similar sternum
but its sacral diapophyses are well dilated.

The Pseudinae are roughly divided into primarily water frogs,
with webs between the toes, and terrestrial, or semiterrestrial,
genera with shorter webs or none at all. The first group of genera
have simple terminal phalanges and are more or less depressed
in form. Considering Telmatobius the central type, Cyclor-
amphus of eastern South America differs from it in that the vomer-
ine teeth are in a line with the posterior edge of the choanae
instead of being between them and, further, in that the males
have a. conspicuous gland on the groin of each side (Fig. 42, B).
Grypiscus of Brazil seems to be a Cyloramphus with caducous
odontoids on the lower jaw. Batrachophrynus of the Peruvian
Andes is certainly a Telmatobius which has lost the maxillary
and vomerine teeth. Calyptocephalus of Chili and Panama has
specialized in the other direction. It may be described as a
Telmatobius with a secondary deposit of bone on the skull, the
skin being involved in the ossification. As in the case of most
frogs which have undergone this type of specialization {e.g.,
Hemiphractus), odontoids appear on the palatines. Pseudis
parallels Chiroleptes of Australia in a disharmonic growth of the
fingers, the first being longer and more or less opposed to the others.
Pseudis has a broad distribution in eastern and southern South
America.

The second group are all more or less terrestrial, except possibly
Hylorina, which differs from all other bufonids in its exceed-
ingly long hands and feet (Fig. 159). The central type here

500

THE BIOLOGY OF THE AMPHIBIA

seems to be Borborocoetes, of wide distribution throughout South
and Central America. It has maxillary and vomerine teeth, very-
short webs (sometimes lacking) between the toes, and non-
dilated digit tips. The terminal phalanges are knobbed or
bluntly T-shaped. Ceratophrys differs from this stock only in
its larger head, more extensive webs between the toes, and simple
terminal phalanges. Zachaenus may be described as a Bor-
borocoetes with a rounded tongue having a flounced or crenulated
edge. Possibly the tongue is highly extensible in life. Zachaenus
is confined to eastern Brazil. Most species have a small, pointed
head. Finally, Eleutherodactylus and Syrrhophus agree closely
with Borborocoetes but have T-shaped terminal phalanges. A

Fig. 159. — Hylorina sylvatica, a Chilean bufonid.

few species of Eleutherodactylus have extensive webs and others
have none at all, some have broad digital discs and others appar-
ently (but not actually, as shown by their histology) lack these
adhesive discs. Syrrhophus is merely an Eleutherodactylus
without vomerine teeth.

The history of the Pseudinae cannot be followed in the fossil
record. Only Ceratophrys has been described as a fossil and
this from the Pleistocene of Brazil.

Subfamily 4. Rhinophryninae. — The Mexican burrowing toad,
Rhinophrynus, is so highly specialized that it may well be isolated
in a subfamily distinct from the Pseudinae with which it seems
to have the closest affinities. Its pectoral girdle alone is dis-
tinctive, the omosternum being rudimentary and the sternum
entirely lacking. Teeth are lacking and the tongue is peculiar
in that it is free anteriorly and apparently protrusible in mammal,
rather than in frog, fashion. A close parallel occurs in the African

RELATIONSHIPS AND CLASSIFICATION

501

bufonid Werneria. Rhinophrynus dorsalis is a round-bodied,
smooth-skinned toad with a very small pointed head. Its
coloration of pink and brown gives it a somewhat pathological
appearance. Its toes are partly webbed, and an enormous
cornified tubercle or " spade" covers the prehallux. The first
toe is peculiar in that it possesses only one phalanx beyond the
metatarsal and this is converted into a shovel-like segment. The
sacral diapophyses are only moderately dilated. It is remarkable
that the burrowing Salientia of the same body form as Rhinophry-
nus may have either cylindrical, slightly dilated or enormously
dilated sacral diapophyses. Rhinophrynus, like many other
specialized burrowers, feeds largely on termites.

Subfamily 5. Bufoninae: True Toads. — Bufonidae without
maxillary teeth, sacral diapophyses dilated, sternum cartilaginous

Fig. 160. — Nectophrynoides vivipara, a viviparous toad of East Africa.

or calcified, omosternum absent or, if present, cartilaginous. The
Bufoninae represent very probably an unnatural group of toads
showing closest affinities to the Criniinae. Except for Bufo,
they are confined to Africa and southern Asia. The most primi-
tive genus is Nectophrynoides (Fig. 160) of East Africa, which
differs from Pseudophryne of Australia in its larger head, wider
sacrum, and larger omosternum. Further, its vertebral column
is typically procoelous, the notochord is not retained, and the
intervertebral discs are not loosely attached as in Pseudophryne.
It differs remarkably from Pseudophryne in embracing the only
ovo viviparous Salientia in the world (see page 74). Necto-
phryne of Africa, the Malay Peninsula, and the western part of the
Indo- Australian Archipelago differs in the loss of the omosternum,
and in the flattened, T-shaped terminal phalanges (spatulated).
Some of the East Indian species seem to grade into Bufo (Fig.

502 THE BIOLOGY OF THE AMPHIBIA

161), but the majority are broad-webbed, arboreal forms. Two,
perhaps all, of the African species have broad lamellae on the

Fig. 162. — The enlargement of the articular tubercles to form pads. A. Phryn-
ella pulchra. B. Nectophryne afra. S.P., sub-articular and palmar pads.

under surface of the hands and feet (Fig. 162). It is highly prob-
able that the non-lamellated African species are referable to Necto-
phrynoides. The African Werneria is of uncertain affinities. It

RELATIONSHIPS AND CLASSIFICATION

503

was described with a tongue free in front, as in Rhinophrynus.
The genus is known only from the type. The Asiatic Pseudobufo
is especially distinctive. It is a large, rough-skinned water toad
(Fig. 163), known from the Malay Peninsula, Sumatra, and
Borneo. It is distinguished by its extensively webbed toes and
upwardly directed nostrils.

The last genus in the subfamily is the common toad Bufo.
The distribution of this genus is world-wide except for New
Guinea, Polynesia, Australia, and Madagascar. As in the
case of Pseudobufo, its immediate relatives are unknown. It

Fig. 163. — Pseudobufo subasper, an aquatic toad of India.

is not improbable, however, that Bufo descended from a toothed
ancestor, for a tooth ridge develops in the tadpole, as shown
by Oeder (1906). Bufo is distinguished from the other genera
in the subfamily by a combination of characters: simple terminal
phalanges, laterally directed nostrils, and partly webbed toes.
Nevertheless, it seems to grade into both Nectophryne and
Nectophrynoides. Some African species, such as B. preussi, have
a smooth skin and possess an omosternum. Most species of Bufo
lack the omosternum, are rough-skinned, and possess large para-
toid glands. Bufo micronotus has the blunt, subspatulate ter-
minal phalanges and the large eggs of Nectophrynoides, although
it has the external appearance of a Bufo.

504

THE BIOLOGY OF THE AMPHIBIA

Fossil toads are not sufficiently numerous or complete to show
how Bufo and related Bufoninae diverged in time. Most of the
fossils come from the Miocene and later formations of Europe.
Platosphus, Diplopelturus, Pliobatrachus, and Bufavus are of
uncertain affinities.

Subfamily 6. Elosiinae. — Bufonidae with a pair of scute-like
structures on the upper surface of each digit tip, the latter more
or less dilated; omosternum and sternum cartilaginous; terminal
phalanges T-shaped. The Elosiinae include three genera, Elosia,
Megaelosia and Crossodactylus, all confined to eastern Brazil.
Crossodactylus is merely an Elosia without vomerine teeth.
It is represented by three species. Megaelosia is a giant Elosia
having very small pseudoteeth (bony processes) on the lower jaw,
a raised palatine ridge, and elongated maxillary teeth. Megae-
losia, which is perhaps hardly generically distinct from Elosia,
is interesting as illustrating the first stage in the development of
pseudoteeth. These structures have appeared again and again
in the Salientia and have until recently been called "true teeth."
While their ontogeny has never been studied, their incipient stages
are represented in such genera as Megaelosia and Genyophryne.

The Elosiinae seem to have arisen from some genus of Pseu-
dinae, probably from Borborocoetes. They are of especial
interest as forming the ancestral stock from which the Dendro-
batinae have arisen. Although themselves not rich in species,
they have apparently given rise to one of the dominant sub-
families of neotropical Salientia.

Subfamily 7. Leptodactylinae. — Bufonids with a narrow, bony
sternum, either entire or divided at the posterior end. The
Leptodactylinae are South American, a few species extending
into Central America and the West Indies. The primitive mem-
ber of the subfamily seems to be Physalaemus, which has the
broadest sternum of all and seems to have arisen directly from
Borborocoetes. The species of this genus were formerly
referred to Paludicola, a genus which has recently been divided
into three genera by Parker (1927). Physalaemus differs from
Pleurodema in possessing a quadratojugal. Eupemphix is a
Physalaemus which has lost the maxillary teeth. Limnomedusa
is a large, slim Physalaemus with a vertical pupil. Leptodactylus
(including Plectromantis) is a Physalaemus with the omosternum
ossified. Edalorhina is a brightly colored Physalaemus with the
tympanum very distinct. Thus, all the genera of Leptodacty-

RELATIONSHIPS AND CLASSIFICATION

505

linae are merely slightly modified members of the Physalaemus
stock. Paludicola, in the broad sense, is such a widespread
stock, of such varied body form and color, that it affords a possible
ancestor for the other groups. Leptodactylus is the most
dominant group of Leptodactylinae. It includes the so-called
" South American Bull Frogs." Most of the species are Rana-
like in appearance except for their prac-
tically webless toes. Some species of
Physalaemus resemble some forms of
Leptodactylus closely.

Family 3. Brachycephalidae. — A large
group of small neotropical toads has
recently been shown to be closely allied
to the Bufonidae and to have no relation-
ship to the Ranidae or Brevicipitidae with
which they were formerly confused. They
may be described as Procoela with the
two halves of the pectoral girdle partly or
wholly fused in the midline. They differ
from the Diplasiocoela not only in their
uniformly procoelous vertebral column but
also in their bufonid-like thigh muscles
(the tendon of the semitendinosus passes
ventral to that of the gracilis major and
minor, not dorsal to it, as in the Diplasio-
coela) . The family is primarily terrestrial,
and intercalary cartilages are lacking.
The various genera frequently exhibit
fusions in the vertebrae. In one genus
from Mount Roraima (Oreophrynella),

there are only five presacral segments seventh, eighth, and ninth,
(Fig. 164). The firmisternous condition are fused-
of the pectoral girdle has been assumed at least three times
within the family, once in each of the three subfamilies. The
Brachycephalidae show more clearly than any other family of
Salientia the details of their origin. Each subfamily has arisen
from a different stock of bufonids, but as all the ancestral stocks
were bufonids residing in the same general region, the Brachy-
cephalidae may be considered a natural, even though a com-
posite, family. It is interesting to note that the primitive genus

Fig.
column

quelchii

164.— Vertebral
of Oreophrynella
showing the ex-
treme condition of verte-
bral fusion found in the
Salientia. The first and
second vertebrae, also the

506

THE BIOLOGY OF THE AMPHIBIA

of each subfamily is arciferal to a greater or lesser extent, and
that the specialized ones are firmisternal.

The Brachycephalidae may be readily distinguished from both
ranids and brevicipitids by external characters (Fig. 165). No
ranid other than Rana reached the neotropics, and the only
brevicipitids are Microhylinae and Kalophryninae. The latter

Fig. 165. — Brachycephalid frogs: A. Oreophrynclla quelchii. B. Elosia nasus.
C. Brachycephalus cphippium. D. Dendrobates braccatus.

are mostly small-headed forms resembling the American narrow-
mouthed toads. The Brachycephalidae, on the other hand,
resemble their bufonid ancestors in head form.

Subfamily 1. Rhinodermatinae. — Brachycephalids without
digital dilations or scutes, omosternum and sternum cartilaginous.
Sminthillus, found in Cuba and in both Peru and eastern Brazil,
is only partly firmisternal. It is obviously closely allied to
Syrrhophus (Eleutherodactylus without vomerine teeth) and

RELATIONSHIPS AND CLASSIFICATION

507

retains in all but one species the T-shaped terminal phalanges
of that genus. Geobatrachus is known only from a single
rare species inhabiting high altitudes of the Santa Marta
Mountains in Colombia. It is characterized by its reduced
digits, the outer being lost. Rhinoderma, the last genus, is a
little Chilean frog well known for its breeding habits. The male
carries the eggs and young in his vocal pouch (see page 71).
Rhinoderma may be distinguished from the other genera by its
toothless maxillaries and pointed snout.

Subfamily 2. Dendrobatinae. — Brachycephalids with a pair
of dermal scutes on the upper surface of each digit tip, the latter
more or less dilated into adhesive discs; omosternum present,
frequently bony. The Dendrobatinae have clearly arisen from
the bufonid Crossodactylus or a form closely allied to it. Crosso-
dactylus shows a reduction in width of the coracoid cartilages, the
first step in the development of the firmisternous girdle (Noble,
1926a). It also agrees closely with Hyloxalus in both external
and internal characters. Phyllobates is merely a Hyloxalus
without webs between the toes. Dendrobates is a Phyllobates
without maxillary teeth. These three closely allied genera
inhabit the northern half of South America and Central America.
Phyllobates is represented by about 20 species (Barbour and
Noble, 1920; Dunn, 1924), while Dendrobates has about half
as many forms. They are chiefly forest frogs which frequent
the vicinity of streams, at least when the males are releasing their
charge of tadpoles which they carry on their backs (see p. 70).
Phyllobates is represented by a number of species in the Andes
which are ubiquitous along the edges of small streams.

Subfamily 3. Brachycephalinae. — Brachycephalids without
an omosternum or digital scutes. In two of the four genera the
pectoral girdle is partly fused (Fig. 87), and in the other two
completely so. Dendrophryniscus of Paraguay, northern Argen-
tina, and eastern Brazil includes a number of rough-skinned little
toads, of which the best known is D. stelzneri. Oreophrynella, a
broad-footed form, comes from the top of Mount Roraima in
British Guiana. It agrees with Dendrophryniscus in its partly
fused pectoral girdle. Its vertebral column, however, is much
more specialized. Atelopus is a widely spread genus of often
strangely colored toads. Most South American toads brightly
variegated with black and yellow and having squarish heads and
rather swollen feet, usually prove on dissection referable to

508

THE BIOLOGY OF THE AMPHIBIA

Atelopus. Brachycephalus agrees with Atelopus in its firmis-
ternous pectoral girdle, but its digits are more reduced (Fig.
165, C) and it carries a great calcareous plate on its back often
ankylosed to the neural spines. Brachycephalus is a very small
load known only from eastern Brazil.

Family 4. Hylidae. — The true tree frogs, or Hylidae, may be
described as bufonids with intercalary cartilages and usually
with claw-shaped phalanges (Fig. 166). They are procoelous,
usually with dilated sacral diapophyses. Most, but not all, are
tree frogs. Some, such as the Cricket Frog, Acris, are aquatic,
and others, such as Pternohyla, are terrestrial and more or less
fossorial. There are 16 genera of hylids. All of these save Hyla

Fig. 166. — Arboreal adaptations in the phalanges. Tree frogs have claw-
shaped terminal phalanges which rotate on intercalary cartilages or bones.
Arboreal salamanders may have recurved, spatulated terminal phalanges. A.

Aneides lugubris. B. Hyla ocularis.

are confined to the New World. Two other genera, Hylella and
Nyctimystes, have been described from the East Indian region
(also Australia in the case of the former), but as these genera
are polyphyletic assemblages, scarcely distinct from Hyla, they
are not recognized here. Hyla is spread almost entirely around
the world except for a hiatus in the Indo-Malayan (includ-
ing Borneo), Polynesian, Ethiopian and Madagascan regions.
Hyla arborea meridionalis has been recorded from the Gulf of
Guinea but possibly through error (Noble, 1926). Two hylas
have also been recently recorded from Java. The Hylidae are
divided into two subfamilies.

Subfamily 1. Hemiphractinae. — Hylidae in which the female
carries the eggs on the back, either exposed or enclosed in a
single sac; sacral diapophyses usually cylindrical or slightly

RELATIONSHIPS AND CLASSIFICATION 509

dilated; if well dilated, as in Gastrotheca and Amphignathodon,
a dorsal pouch present in the female; terminal phalanges claw-
shaped. The two subfamilies of Hylidae are sharply distin-
guished only in their modes of life history. The Hemiphractinae
usually have a very slightly dilated sacrum and the skull more or
less roofed over by dermal ossification, while most Hylinae have
a dilated sacrum and little or no dermal ossification. A few large
hylas, however, such as H. taurina, maxima, etc., have the sacrum
scarcely more dilated than Hemiphractus, and several Hylinae,
such as Diaglena and Pternohyla, are noted for their grotesque
casques. The genera of Hemiphractinae are, nevertheless, well
defined and apparently closely related.

Cryptobatrachus (Fig. 20, C) has the appearance of a Hyla,
but its sacral diapophyses are nearly cylindrical. Hemiphractus
(including Cerothyla) has the skull extended into a three-cornered
casque (Fig. 168, A). It also possesses pseudoteeth on the lower
jaw and palatines. Gastrotheca is not known to have any
character save the dorsal pouch to distinguish it from all species
of Hyla. In fact, the males of the various species of Gastrotheca,
lacking the pouch, have been repeatedly described as "new
species" of Hyla. Amphignathodon is a Gastrotheca which has
redeveloped true teeth on the lower jaw. Amphignathodon is
said to lack the omosternum, but it is actually present, the
pectoral girdle resembling that of Gastrotheca closely. Crypto-
batrachus and Gastrotheca are widely spread over northern
South America; Hemiphractus occurs in Brazil, and north-
western South America including Panama; while Amphignatho-
don is known only from Ecuador.

The most remarkable osteological feature of the Hemiphractinae
is the redevelopment of true teeth on the dentary of Amphigna-
thodon. Such teeth do not occur in any other Salientia, the
toothlike structures on the lower jaw of Ceratobatrachus,
Dimorphognathus, etc., being mere bony processes from the
jawbones without the characteristic features of teeth. May
these teeth of Amphignathodon be considered atavistic struc-
tures— a reminiscence from Branchiosaur ancestors of the frogs?
There does not seem to be any other satisfactory explanation for
their sudden appearance in the specialized Amphignathodon.

The best known Hemiphractinae are the Marsupial Frogs.
Because of the dictates of priority, this group long known by the
appropriate name of "Nototrema" must be called "Gastro-

510

THE BIOLOGY OF THE AMPHIBIA

theca," although the theca, as stated above, is on the back not
on the belly. There are three main types of Marsupial Frogs.
In G. pygmaea the opening of the sac is represented by a long
slit extending the length of the back. In G. ovifera and its
allies the sac opens by a narrow mouth in the sacral region, the .
eggs are large, and the young escape fully formed from the
pouch. In the last group, represented by G. marsupiata and
closely allied species, the pouch is the same as in ovifera but the
eggs are smaller and more numerous. The young hatch out as
tadpoles. Marsupial Frogs have the skull more or less covered
by a secondary deposit of bone. In a few forms such as G.
weinlandii the derm of the back is studded with numerous cal-
careous plates. In these species the young, during their sojourn
on their maternal parent's back, are safely enclosed within a
veritable coat of mail!

Subfamily 2. Hylinae. — Hylidae in which the eggs are laid
in or near the water; sacral diapophyses dilated; terminal pha-
langes claw- or T-shaped. There are 12 valid genera of Hylinae
and at least 3 others which are sometimes recognized. All of
these are closely allied to Hyla and differ in very few characters.
The most distinct are the neotropical Centrolene and Centrol-
enella, which have T-shaped terminal phalanges and frequently
truncated- digital discs. The recently described Allophryne
is a toothless Centrolenella with peculiar scale-like patches of
roughened epidermis strewn over head and back. The American
Acris and particularly Pseudacris are not distinguished from
Hyla by any structural characters. Pseudacris (Fig. 167) is
merely a group of Hyla species with reduced webs. Microhyla,
Eleutherodactylus, and various other natural genera include
species with and others without webs on their toes. Acris
is a Rana-like Hyla, aquatic or terrestrial but never arboreal.
There are a number of neotropical hylas with small digital dila-
tions similar to those of Acris, but none is so Rana-like. In the
Australian regions, however, there are a few hylas which resemble
Rana even more closely than Acris does. H. nasuta of Queens-
land, in form, color, dorsal folds, etc., is remarkably similar to
R. mascareniensis. Further, its intercalary cartilages are greatly
elongated as in Acris. It would seem that terrestrial life has
called forth a greater development of these primarily arboreal
structures (see page 95).

RELATIONSHIPS AND CLASSIFICATION

511

Amphodus (including Lophyohyla) may be described as a Hyla
which has developed pseudo teeth on the lower jaw and para-
sphenoid. In Amphodus both dentary and prearticular are
extended into a ragged sawtooth edge. Its palatines are simi-
larly edged but the projections are not so elevated. The para-
sphenoid odontoids form a broad patch and many are fused
together producing oblique ridges. Similar odontoids occasion-

Fig. 167. — Several species of hylids lack webs between their toes and do not
climb. The American species are frequently referred to the genus Pseudacris.
Hyla triseriata (A) is a typical Pseudacris, while H. ocularis (B) climbs readily,
especially up grass stems and bushes.

ally occur in other genera of Hylinae. In Hyla (Nyctimantis)
rugiceps they occur on the prevomers together with the true
vomerine teeth. The sacrum of Amphodus is moderately dilated
and its ovarian eggs are small and densely pigmented. It has,
therefore, probably no close affinity to Hemiphractus, which has
developed similar bony extensions of the lower jawbones. Amph-
odus is known from Trinidad and Brazil.

A third group of Hylinae are characterized by the development of
excessive bony growths on the skull. In these, strangely enough,
the lower jawbones are not extended into pseudoteeth. A num-

512

THE BIOLOGY OF THE AMPHIBIA

ber of species of Hyla (nigromaculatus, dominicensis, etc.) develop
complete caps of secondary dermal bone to the skull, and in H.
lichenata, and to a lesser extent in nigromaculatus, the occipital
region may be raised into a peculiar bony crown. There is no
doubt, from what has been said concerning the life histories of
these forms (page 67), that they are very closely allied to species
which lack any trace of a secondary bony cover to the skull.
Here and there throughout the neotropics species have developed
more extensive casques than lichenata and these have been
dignified with special generic names. Pternohyla is a small-
disced Mexican Hyla which has extended the secondary bony

Fig. 168. — Secondary ossifications occur in the skin of Salientia. In Pterno-
hyla (B), the ossification forms a thick cover to the skull. In Hemiphractus (A),
this cover is extended to form a pair of broad horns.

growth until it forms in the adult a low ridge along the edge of the
upper jaw (Fig. 168B). Corythomantis is a Brazilian form with
larger discs and more extensive casque. The pupil is said to be
rhombic, as in H. vasta. In Triprion of Mexico the extension of
the casque is carried slightly further, at least it is more sculptured,
and odontoids appear on the parasphenoid and lateral portions
of the palatines. Specimens vary considerably in the number and
extent of these odontoids, but the latter are never very numerous.
Diaglena (including Tetraprion) is identical with Triprion, but
the pupil is said to be horizontal, although, as in H. vasta, this
may be a matter of pupil size at the moment of death. These
helmeted Hylinae are represented by very few species, and
while it is customary to recognize them as distinct genera it is
clear that they are all merely slightly aberrant hylas. Perhaps

RELATIONSHIPS AND CLASSIFICATION

513

the most distinctive is the small Triprion petasatus of Yucatan.
The casque formation in this species has led to a widening of the
ethmoid, a reduction in length of the palatines, and a broadening
of the parasphenoid.

The last group of Hylinae is characterized by a vertical pupil.
This is not a good character, for it has arisen independently in
H. vasta and in H. lichenata of the West Indies (see page 89),
also independently — to judge from the numerous differences
which distinguish grand from papua — in the two Papuan species
which have been linked together under the name of "Nyctimy-
stes." In general, pupil form does not seem a reliable character
in the Hylidae to distinguish related groups of species, for in this

Fig. 169. — Phyllomedusa bicolor, a South American tree frog possessing both
opposable thumbs and inner toes.

family the pupil has changed its form too frequently. There is,
however, one group of neotropical Hylinae which has added to
the pupil character certain other features which seem to distin-
guish them as a natural group of species. These species are
referred to Phyllomedusa (including Agalychnis). They are
hylas which have developed a bright green color (sometimes
brown in young), usually a red iris, a vertical pupil, and, most
important of all, a disproportionate growth of the toes. The
more primitive species, moreleti, calcarifer, and spurrelli, differ
from Hyla in toe proportions, the disc of the first reaching the
base of the disc of the second and not falling much short of this
point, as in Hyla. They have broadly webbed toes and look like
large specimens of Hyla uranochroa or H. pulchella except for their
pupil form and toe proportions. The other species of Phyllome-
dusa show more or less reduction of the webs, an elongation of the

514

THE BIOLOGY OF THE AMPHIBIA

first toe, a shortening of the second, together with a slight
twisting of the first, until in the most specialized forms it opposes
the other toes. The extreme species lose the digital dilations
entirely, reduce the intercalary cartilages to thin wafers, and
develop large parotoid glands (Fig. 169). There are no less than
18 species of Phyllomedusa distributed from Argentina to Mexico.
They are very handsome and sometimes grotesque tree frogs.
One of the most attractive is P. perlata, which has its paratoid
glands extended along each side of the body as a row of pearl-like
beads. The life history of the species of Phyllomedusa is distinc-
tive and nearly uniform throughout the group (see page 69).

The genus Hyla is one of the largest and most stable groups of
Salientia. It is remarkable that Hyla, as well as such different
types as Rana and Bufo, are almost the only Salientia which have
succeeded in spreading widely over both hemispheres. The his-
tory of these migrations is practically unknown. Only one fossil
Hyla has been described. This is from the Miocene of Europe.

SUBORDER 5. DlPLASIOCOELA.— The true frogs, ranids; Old
World tree frogs, polypedatids; and narrow-mouthed toads,
brevicipitids, are closely allied. They have been grouped
together in the suborder Diplasiocoela. The latter is defined as
a primary group of Salientia having the centrum of its sacral
vertebra convex anteriorly and with a double condyle posteriorly
for the coccyx, the eighth vertebra biconcave and preceded by
seven procoelous vertebrae (the first two rarely fused). The
thigh musculature is always of the most specialized type (semi-
tendinosus distinct from the sartorius, its distal tendon passing
dorsal to the distal tendon of the gracilis mass). A few Diplasio-
coela retain the uniformly procoelous vertebral column of the
Procoela, but their thigh musculature remains specialized as
evidence of their relationship. The Diplasiocoela include the
most specialized of all Salientia. They are all firmisternal,
without ribs, and therefore differ strikingly from most other
Salientia except the Brachycephalidae. The latter are purely
neotropical, and as the genera of Brachycephalidae are well
defined, they should not be confused with the Diplasiocoela.

The suborder is cosmopolitan but each of the three families
seems to have had its own center and time of dispersal. The
Ranidae represents the most primitive stock. It gave rise
on one hand to the Polypedatidae and on the other to the
Brevicipitidae.

RELATIONSHIPS AND CLASSIFICATION

515

Family 1. Ranidae. — The true frogs are the most primitive
Diplasiocoela. They are distinguished from the other two
families in the suborder by their cylindrical or slightly dilated
sacral diapophyses and digits without intercalary cartilages
(Fig. 50). Ranids are primarily Old World frogs. Only one
genus, Rana, reaches America. No ranid is found in Australia,
except a representative of the same genus. Africa seems to have
been a center of differentiation for ranids. Four of the six
subfamilies are confined to this region. The other two are
either peculiar to southern Asia, the East Indian and Polynesian
islands, or are found in this region and in Africa. Rana is known
as a fossil from the Miocene and later formations of Europe.
Probably other described fossils, such as Ranavus and Aspherion,
are not generically distinct from Rana. The fossil record throws
very little light on the origin of the many genera of Ranidae.
Emphasis must necessarily be laid on the anatomical characters
in seeking relationships.

Subfamily 1. Arthroleptinae. — Small African ranids possess-
ing horizontal pupils and lacking vomerine teeth. Arthroleptis
and Phrynobatrachus are almost identical with Rana except for
their small size and dentition. They are widely spread over
Africa and are represented by many species. Cardioglossa of the
rain forest and Schoutedenella of the Katanga, Africa, have
apparently arisen independently from different stocks of Arthro-
leptis by a loss of their maxillary teeth. Dimorphognathus is
closely related to Arthroleptis batesii, but the male possesses long
pseudoteeth on the mandible (Fig. 40, B). Two of the six
genera of Arthroleptinae are said to exhibit a cartilaginous
instead of a bony sternum. This distinction may not prove to be
a good one, for in most of the small species the sternum is more
or less cartilaginous, while in the large species it tends to be bony.
In most forms the sternum is short, but in the recently described
Arthroleptella it is long and bony. This genus seems to be
hardly distinct from Arthroleptis.

The Arthroleptinae represent a natural group of genera in
spite of the differences of dentition or ossification of the sternum.
In some species of Arthroleptis, in Schoutedenella (Fig. 170) and
in Cardioglossa the third finger of the male is greatly elongated.
This secondary sexual character is not found elsewhere in the
Amphibia. Just as in Rana, some species of Arthroleptis and
Phrynobatrachus have their digit tips more or less dilated.

516

THE BIOLOGY OF THE AMPHIBIA

Correlated with this, the terminal phalanges may be more or less
T-shaped. Every intergrade exists between the extremes. The
pectoral girdle exhibits either a A-shaped or an unforked
omosternum. The vertebral column is sometimes entirely
procoelous. The range of variation in Arthroleptis and Phry-
nobatrachus is closely paralleled by that in the genus Rana,
except that the vertebral column is never normally procoelous
in any species of Rana.

Arthroleptis and Phrynobatrachus form one of the dominant
elements in the frog fauna of Africa. They are tiny frogs which

Fig. 170. — Schoutedenella globosa, male with the elongate fingers characteristic of

his sex.

hop about on the forest floor or among brush in the more open
country. The eggs of two species of Phrynobatrachus are known.
They are laid in pools while one species of Arthroleptis (steno-
dactylus) lays its eggs in shallow burrows on land. When the
life histories of more species are known it may be possible to
distinguish Phrynobatrachus from Arthroleptis on the basis
of life-history differences.

Subfamily 2. Astylosteminae. — West African ranids of
average size, having a vertical pupil, a bony omosternum forked
posteriorly, a broad cartilaginous or calcified sternum, and
usually broad, calcified coracoid cartilages ("epicoracoid carti-
lages"). Three of the four genera have the terminal phalanges of
two or more toes bent sharply downward and perforating the

RELATIONSHIPS AND CLASSIFICATION

517

integument. The subfamily includes three monotypic genera
from Spanish Guinea and the Cameroons : Scotobleps, Nyctibates,
and Gampsosteonyx ; also a fourth genus containing three
species, all from the same region. The latter genus, Astylo-
sternus, includes the famous " Hairy Frog," A. robustus, a species
with a peculiar growth of villous processes in the male (see page
164).

There can be little doubt but that the Astylosterninae embrace
a natural group of closely related species (Noble, 1924a) . It is,
therefore, interesting to note the evolutionary change which has
taken place within this subfamily. The primitive Nyctibates
and Scotobleps have the toes three-fourths webbed, the more
specialized Astylosternus, slightly webbed, and Gampsosteonyx,
free. In Nyctibates the terminal phalanges of both fingers and
toes are simple and only slightly curved. In Scotobleps the
fingers are as in Nyctibates, but the terminal phalanges of the
second and third toes are long, sharply pointed, and bent down-
ward at almost a right angle (Fig. 30). The points of these
extraordinary " claws" may or may not perforate the integument
of the toe tip. In Astylosternus robustus three toes are bent in the
same peculiar way, only the first and fifth retaining terminal
phalanges of the usual form. In Astylosternus diadematus the
terminal phalanges of all five toes are slightly bent and perforate
the derm; those of the fingers are slightly curved and swollen at
the tips but not very different from the finger phalanges of
Nyctibates. In Gampsosteonyx the toes are modified exactly
as in A. diadematus. Just distal to the bent phalanges of
Astylosternus, Gampsosteonyx, and apparently the others, there
is embedded in the digit tip a nodule of bone which, to judge
from its position, may have had its origin in the same blastema
as the phalanges.

These extraordinary bent phalanges of the Astylosterninae are
found elsewhere among Salientia only in certain African species
of Rana (R. mascareniensis, R. christyi, etc.), where in all proba-
bility they had an independent origin. It is difficult to imagine
any function for these structures. It is possible that they could
give their owners a surer grip before leaping. But if so, why is
the perforation of the derm such a haphazard matter? On
further study the impression grows that these are abnormal
structures carried along by the species, because they are not
actually detrimental to the existence of their owners. Whatever

518

THE BIOLOGY OF THE AMPHIBIA

is the functional significance of these structures, it is important
to note their genesis. They did not evolve gradually in the
phylogenesis of the group, but first two toes, then three, and then
five were fully transformed.

Nothing is known of the detailed habits of the AstylOsterninae.
All the species are apparently forest frogs, and A. robustus at least
must frequent mountain streams, for its tadpole is modified for
life in swift streams. Scotobleps, however, has a tadpole of the
polliwog type. . The dermal papillae surround its mouth only
below and on the sides, while the larval tooth formula is 1, 1-1,

i-i // i-i, i-i, i.

Subfamily 3. Phrynopsinae. — Small Rana-like African frogs
with horizontal pupils and vomerine teeth but a cartilaginous
unforked omosternum and sternum. Phrynopsis is readily
recognized by its large head with elongated, spike-like teeth.
Leptodactylodon has a small head and slightly dilated digital
discs. The elongated teeth of Phrynopsis are single pointed, not
bifid as those of Rana. Such teeth appear elsewhere in the
Salientia; chiefly in the large-headed forms such as the larger
species of Ceratophrys or in a few broad-headed forms, as
Leptopelis brevirostris (see page 125).

Phrynopsis is known from two species: boulengeri of Mozam-
bique and ventrimaculata of the Cameroons. Leptodactylodon
is represented by three species, all confined to the Cameroons.
None of the species is common in collections.

Subfamily 4. Raninae. — Ranids with a bony sternum, pointed
or slightly dilated digit tips, no discs on either the upper
or lower surfaces of the digital dilations when the latter are pres-
ent. The Raninae include Rana and its close allies. Several
of these have been described as possessing a cartilaginous
sternum. It is nevertheless bony in adult specimens. The
Raninae have the same extensive range of the family. This is
because the subfamily includes the widespread Rana. The other
six genera of Raninae have a very local distribution either in
Africa or in southern Asia and the adjacent islands.

It is uncertain which genus of the subfamily approaches most
closely to the stock from which the Raninae were derived.
Nevertheless, all the genera may be defined by contrasting them
with Rana. Nyctibatrachus is a small Rana with a vertical
pupil. It has small discs and a slightly forked bony omosternum.
Nyctibatrachus is known from four species, all Indian. Nanno-

RELATIONSHIPS AND CLASSIFICATION

519

batrachus includes a single species inhabiting Malabar. It may-
be described as a small Rana having a squarish pupil. Nanno-
phrys embraces two small chunky species from Ceylon. These
have a cartilaginous omosternum (bony sternum) and slightly
dilated sacral diapophyses; otherwise they are identical with
Rana. Oreobatrachus is merely a Bornean species of Rana
which has lost the vomerine teeth. A parallel change has
occurred in certain Asiatic and Central American species of Rana
but these are not considered distinct genera. Oreobatrachus
differs, however, from Rana in having a weak ridge between the
Eustachian tube openings and a tongue less prominently notched
posteriorly. It is a matter of opinion whether these can be
considered valid generic differences. In fact, all of the small
genera seem to be merely local specializations of a Rana stock.

The well-known water frog Oxyglossus, now known by the
name of "Ooeidozyga," seems at first glance to be merely
another case of a Rana without vomerine teeth. Its sternum
in the adult is bony and the omosternum is bony and A-shaped.
But its tongue is entire and pointed posteriorly except in the
recently described semipalmata and sometimes in laevis. The
notched tongue of these species represents a distinct approach to
Oreobatrachus. Further, two species of Ooeidozyga have the
same type of tadpole, readily distinguished from that of any
species of Rana by its peculiar mouth (lips small, papillae
and teeth absent, and dorsal fin folded to varying extent).
Ooeidozyga has a wide range from southern China and ;he
Philippines to Bengal and the western part of the Indo- Australian
Archipelago, including Borneo and the Celebes.

Two large African frogs seem closely allied to one another and
closely related to Rana. Gigantorana, which includes only the
largest frog in the world, yoliath, is perhaps not generically distinct
from Rana. It differs, however, in that the coracoid cartilages
("epicoracoids") anterior to the coracoids are only weakly calci-
fied. Its toes are extensively webbed and end in thick dilations.
Conraua, also known from only a single large species restricted
to the Cameroons, as in the case of goliath, has the same weakly
calcified coracoid cartilages and extensively webbed toes tipped
with thick dilations. Conraua differs from Gigantorana in its
small tongue, unnotched posteriorly.

The enormous genus Rana has spread over the entire world
except the southern part of South America, the southern and

520

THE BIOLOGY OF THE AMPHIBIA

central parts of Australia, New Zealand, and eastern Polynesia.
Numerous species of Rana occur in each continent except South
America and Australia. The species agree well in general body
form, although some are fossorial, others primarily aquatic, and
still others terrestrial. The skeleton does not remain uniform
throughout this series. This is especially true in Africa where
some species assigned by Boulenger (1918) to a separate sub-
genus Ptychadena have the clavicles greatly bent aud closely
approaching the coracoids. Another group of species, many of
which are burrowers, have the clavicles similarly bent and
extremely narrowed. They are placed by Boulenger in another
subgenus, Hildebrandtia. It is possible that these subgenera
represent natural groups of species. In other genera, however,
natural groups of species may also be picked out. The use of the
subgeneric names has not yet become a practice in herpetology,
and for the sake of uniformity they are not used here.

Three of Boulenger's subgenera of Rana from the East Indian
and Asiatic regions have been raised to genera, for, although
they are only slightly different from Rana, they represent
the first divergence of a stock which eventually gave rise to the
Polypedatidae. They are placed in a subfamily distinct from the
Raninae in order better to represent this divergence. It is,
therefore, not so much the degree of structural divergence as
the mutual relationships which determine the final taxonomic
assignment of a species.

The recently described Altirana is a Rana with broad, partly
ossified sternum, a cartilaginous omosternum, a slightly notched
tongue, and no vomerine teeth. It is known only from Tingri,
Thibet.

Subfamily 5. Petropedetinae. — African ranids with a pair
of dermal scutes on the upper surface of each digit tip. The
two genera in the subfamily are readily distinguished by their
size and palates. Arthroleptides is much larger than Petro-
pedetes and lacks the vomerine teeth.

The skeleton of the Petropedetinae agrees closely with that
of the Raninae. The omosternum is bony and either entire
or slightly forked posteriorly. The terminal phalanges are T-
shaped.

Dermal scutes apparently identical with those of the Petro-
pedetinae have been redeveloped in one of the subfamilies of
Brachycephalidae. This adds one more to the many cases of

RELATIONSHIPS AND CLASSIFICATION

521

parallel evolution in the Salientia. Incipient scutes (grooves)
are found in certain brevicipitids and bufonids. They have
no known function.

Arthroleptides is known from a single species, martiensseni,
from Tanganyika Territory. Petropedetes is believed to include
five valid species from the Cameroons and Sierra Leone. The
latter show considerable diversity in the extent of digital webbing.
Very little is known of the habits of these frogs. The ovarian
eggs of P. palmipes are under a millimeter in diameter and
densely pigmented. This suggests that the eggs are laid in the
water. The tadpole of one species has been described.

Subfamily 6. Cornuferinae. — Ranidae with digit tips more
or less dilated and showing, either as a groove around the edge
or as a complete disc on the ventral surface of each, some indica-
tion of the friction pad which characterizes the digital dilation
of Polypedates. The 10 genera which comprise the Cornu-
ferinae extend from Southern China, the Philippines, the Fijis
and Solomons, westward across New Guinea and the Indo-
Australian Archipelago to India; one genus, Hylarana, reaching
Africa and northern Australia. The Cornuferinae have arisen
from Rana in different parts of the range. They represent
a very uniform group. Some of the genera apparently grade
into others, making the limits of these groups almost impossible
to define.

The widespread Hylarana is most closely allied to Rana and
may not represent a natural group. It retains an unforked
omosternum, as do most species of Rana. Its toes and usually
the fingers have the upper surface of the digital dilations separated
from the lower by a groove. Its tadpole and life history agree
closely with those of Rana, although one species lays its eggs out
of water, the beginning of an egg-laying habit which characterizes
Polypedates (see page 66).

Micrixalus is merely a group of small species of Hylarana
lacking vomerine teeth. Micrixalus is known from eight species
distributed from Hainan and the Philippines to India. It grades
into Staurois and differs from some species of that genus only in
its Rana-like tadpole.

Staurois, as recently defined by Boulenger (1918a), would
differ from Hylarana and Micrixalus only in that the friction pad
on the ventral surface of each digital dilation is completely
surrounded by a groove. An examination of these pads under a

522 THE BIOLOGY OF THE AMPHIBIA

high magnification reveals that this distinction of incomplete
vs. complete pads breaks down entirely. The cross-groove
may be present or absent in different specimens of Staurois
hainanensis. S. natator and S. tuberlinguis frequently lack
the cross-groove, which is usually present in S. nubilis. On
the other hand, on turning to the life history it is found
that all species of Staurois recognized by Boulenger and some
species of "Hylarana" have a highly specialized mountain-
brook tadpole. In no other Salientia is there developed a large
adhesive disc on the ventral surface of the tadpole's body just
posterior to the mouth. It is shown above (page 62) that
specialized larval structures may point as surely to species
relationship as specialized adult structures. It is, therefore,
advisable to redefine the genus Staurois in order that it may
include all species having this same distinctive tadpole. Staurois
may be considered to include a large series of species from
Hainan, the Philippines, Borneo, and the Malay Peninsula,
Sumatra, Java, Burma, and Siam. These have an unforked
(or slightly notched) omosternum, nasals separated from each
other and from the frontoparietal, and tadpole with a large,
adhesive belly disc. The vomerine teeth may be present or
absent; the friction discs on the ventral surface of the digital
dilations may be completely or incompletely surrounded by a
groove. In most features (pupil form, digital webbing, etc.)
Staurois agrees with Hylarana. Under this definition many
species formerly referred to Hylarana are placed in the genus
Staurois. This applies to whiteheadi, livida, cavity mpanum,
hosii, jerboa, afghana, etc.

Although Staurois in its skeleton approaches most closely to
Polypedates and may have given rise to that genus, another group
of Cornuferinae parallel Staurois in the development of a partial
or complete friction pad. These genera differ from Hylarana,
Micrixalus, and Staurois in their omosternum, which is forked
posteriorly. The least specialized of them seems to be Platy-
mantis, which has only a lateral digital groove as in Micrixalus.
It differs from the latter in its larger size, persistent vomerine
teeth, and forked omosternum. Further, its toes are free or
slightly webbed. The digital dilations of Platymantis may be
very small. One species, solomonis, has the lateral groove only
on the toes, the finger tips lacking it entirely. It is very likely
that Platymantis arose directly from Rana and has no relation-

RELATIONSHIPS AND CLASSIFICATION 523

ship to Micrixalus. It has a wide distribution in the Philippines,
Halmahera, Kei Islands, New Guinea and neighboring islands,
New Britain, the Solomons, and the Figis.

Discodeles of the Solomon Islands and the Fijis differs from
Platymantis only in that the tongue bears an obtuse papilla in
its center and that the toes are extensively webbed. In Cornufer
the digital dilations are much larger than in either Platymantis or
Discodeles and the friction pads are complete, that is, a cross-
groove marks off a disc on the ventral surface of each dilation.
Cornufer has, therefore, attained the same type of digital pad
specialization found in Staurois and Polypedates. It is not
closely related to these genera, for its toes are only slightly
webbed, its omosternum is forked, and its nasals are large
and in broad contact. Cornufer is found in Burma, the Philip-
pines, Borneo, and the Solomon and Fiji Islands.

Ceratobatrachus was referred in earlier classifications to a
distinct family of its own, for it was supposed to possess teeth on
the lower jaw. These so-called " teeth" are merely excess
bony growths of the lower jawbones. A similar modification has
occurred in various families of Salientia. Ceratobatrachus
guentheri is obviously related to Platymantis solomonis. They
are both large-headed species with small discs and short webs
between the toes. Their shoulder girdles are essentially alike.
The skulls differ, however, for Ceratobatrachus has a secondary
deposit of bone roofing the squamosal and ethmoid regions.
Pseudoteeth appear on the lower jaw but no odontoids are present
on the palatine, as in most frogs which have undergone a similar
specialization. There is hardly any more difference between
Ceratobatrachus guentheri and Platymantis solomonis than between
the species of Chiroleptes or Ceratophrys having a complete
secondary skull roof and those species of the same genera without
this bony elaboration. Ceratobatrachus, however, has gone
farther than these forms in the development of pseudoteeth along
the lower jaw. Both guentheri and solomonis occur in the same
locality. The former is confined to the Solomons.

The life history, as far as it is available, confirms the relation-
ship as outlined above. Guentheri and solomonis have large eggs.
Discodeles and Cornufer practice direct development (see page
64), and the encapsuled froglet before hatching is characterized
by certain apparently distinctive structures.

524

THE BIOLOGY OF THE AMPHIBIA

There remain in the Cornuferinae three monotypic genera to
discuss. All of these are very rare, disced species allied to
Cornufer but lacking vomerine teeth and webs between the toes.
Batrachylodes of the Solomons, like many other species which have
lost the vomerine teeth, is a dwarf form. Simomantis of Borneo
seems to be a Staurois with webbed fingers. Its omosternum is
unforked, and vomerine teeth are absent. It has a typical
Polypedates pad on the ventral surface of the digits and also
a groove on the dorsal surface. Palmatorappia of the Solomons
seems to be a case of parallel evolution in a different stock,
namely in Cornufer or an allied genus. Its omosternum is
forked. It may be described as a Cornufer with extensively
webbed fingers and toes.

Fig. 171. — Polypedates dennysi, a tree frog of southeastern China.

Family 2. Polypedatidae. — The diplasiocoelous frogs with
cylindrical sacral diapophyses and intercalary cartilages represent
very probably a natural family which has evolved from the Ran-
idae in much the same way that the Hylidae did from the Bufoni-
dae. They are distinguished from ranids only by the presence
of the intercalary cartilage. The 13 genera in the family are not
regrouped into subfamilies, for they represent too uniform a
stock. The Polypedatidae inhabit southern Asia, Japan, the
Philippines, the East Indian Islands, Africa, and Madagascar.

It has been frequently claimed that the Polypedatidae do not
represent a natural group but that ranid stocks in different parts
of the world have independently developed an intercalary carti-
lage. This is certainly not true in Africa, where Chiromantis,
Leptopelis, Hylambates, Hyperolius, Megalixalus, and Kassina

RELATIONSHIPS AND CLASSIFICATION

525

show in their skeletal and external anatomy closer affinity to one
another than to any other African ranids. Further, the Mada-
gascan Mantidactylus, Aglyptodactylus, Hemimantis, and Man-
tella are very closely allied and seem to have arisen from the same
polypedatid ancestor as the African genera. Polypedates
(Fig. 171) differs anatomically from Staurois (as defined here)
only in the presence of the intercalary. But it differs remarkably
in life history and it is not improbable that the resemblance may
be due to convergent evolution. Whether or not Polypedates
arose from Staurois, the anatomical evidence at present available
points toward the Polypedatidae as being a natural group.

Most of the Polypedatidae are tree frogs. A few have given up
their arboreal habit and have returned to the sod while retaining
almost the entire digital adhesive mechanism of their relatives
(see page 95).

The most primitive genus in the family is the widespread
Polypedates which inhabits the entire range of the family except
Africa. It has a horizontal pupil, an entire or slightly notched
omosternum, and a long, bony sternum. Its terminal phalange,
may be either bluntly or broadly Y-shaped. Philautus has
arisen from Polypedates in many parts of its range by that ofts
repeated process, a loss of the vomerine teeth. Most species of
Philautus are small and have the metatarsals more or less united-
while the species of Polypedates are larger and usually have
more distinct webs between the metatarsals. Phrynoderma is a
Burman Polypedates which has lost its vomerine teeth and
reduced its tongue until it lacks any suggestion of a notch behind.

The African Chiromantis is very closely allied to Polypedates,
differing only in that the two inner fingers diverge more from the
others than do those of Polypedates. Chiromantis is a tree
frog and has the same breeding habits as Polypedates. Lep-
topelis, represented in Africa by many arboreal and some
disced terrestrial species, differs from Chiromantis in its vertical
pupil, less diverging fingers, and claw-shaped phalanges. Hylam-
bates has developed a broadly A -shaped omosternum and
its sternum has changed into a broad cartilaginous (or calcified)
plate. It retains the vertical pupil and claw-shaped phalanges
of Leptopelis. Megalixalus may be described as a Hylambates
which has lost its vomerine teeth. The widespread and dominant
genus Hyperolius (Rappia of authors) is merely a Megalixalus
with horizontal pupil. Lastly, the terrestrial Kassina is merely

526

THE BIOLOGY OF THE AMPHIBIA

a Hylambates with very small (apparently absent) digital
discs. A close parallel occurs in the terrestrial species of Lep-
topelis. The widespread K. senegalensis has a small tongue
and frequently lacks vomerine teeth. This has led to its being
described several times as a "new genus and species." It is
remarkable that the arboreal and terrestrial species of Leptopelis
retain the same skeletal organization and differ only in the
extent of the digital dilations. A close parallel, however, occurs
in the species of Hyla.

The Madagascan genera exhibit even a closer affinity to one
another than do the African genera. Polypedates has reached
Madagascar and has apparently given rise to Mantidactylus by a
reduction in width of the terminal dilations and by increasing the
notch in the omosternum until it formed a A. Mantidactylus
retains the same specialized pads of Polypedates, with ventral
and lateral grooves as in the latter. It is sometimes said that
Mantidactylus is merely a Rana which has developed an inter-
calary cartilage. But the discs of Mantidactylus with ventral
pads marked off by a groove do not occur in Rana. Further, the
skull of Mantidactylus, with its small widely separated nasals
and broadly exposed ethmoids, is characteristic of Polypedates.

Aglyptodactylus, including Gephyromantis, is a Mantidactylus
with the metatarsals bound together. It retains the same
femoral glands (Fig. 42, A), a typical secondary sexual character
of Mantidactylus. Hemimantis is a Gephyromantis without
vomerine teeth. Mantella, the most disputed genus in the
series, is a Hemimantis which has lost the maxillary teeth and
reduced the webs between the toes. Mantella has been referred
to the Ranidae and to the "Dendrobatidae" by various authors.
Its true affinities are, however, disclosed by its skeleton. It
possesses an intercalary cartilage, Y-shaped terminal phalan-
ges, A-shaped omosternum, and narrow bony sternum. The
terminal dilations, although small, agree in detailed structure with
those of Polypedates. The webs between the toes may be very
short or absent. In the Hylidae certain genera such as Acris
and Hemiphractus have become secondarily adapted to terrestrial
life. Their digital dilations are reduced greatly in size but
retain the skeletal and histological detail of the broadest hylid
pads. Similarly, the polypedatid Mantella may be considered
a terrestrial tree frog, for its pads, although small, agree with those
of Polypedates.

RELATIONSHIPS AND CLASSIFICATION 527

Family 3. Brevicipitidae. — The narrow-mouthed toads form
a large group of often specialized forms distributed throughout
the Americas, Africa and Madagascar, southern and eastern
Asia, and the adjacent islands including the whole of the Indo-
Australian Archipelago, two genera reaching Queensland. The
less specialized genera agree closely with the Ranidae, differing
only in the more dilated sacral diapophyses. The Brevicipitidae
represent a natural group of genera except for two subfamilies, the
Cacosterninae and the Hemisinae, which seem to have arisen
independently from African ranids. All other brevicipitids
either pass the larval stages within the egg capsule or hatch out
to form a very distinctive tadpole with a median spiracle, a
toothless and expansible mouth, and no external nares until just
before metamorphosis.

The brevicipitid toads exhibit the greatest range of skeletal
modification found in any family of Salientia. Different stocks
have often undergone a rapid and parallel evolution, making it
extremely difficult to recognize natural groups of genera. The
more primitive genera might be considered ranids with the sacrum
more or less dilated, but they differ from most ranids in their
heavy build, large vomers, and ridged palate. The last feature is
remarkably constant throughout the family, only a few genera
lacking the ridges. These ridges are usually described as a pair
of glandular folds, one bounding the entrance to the oesophagus
and the other, smaller and anterior to this, on the roof of the
palate. Sections reveal that neither is more glandular than the
adjacent palate. Both owe their character to a projecting fold
of the connective tissue underlying the mucosa. They may
serve as pads which strengthen the grip on struggling prey. At
least they are not to be confused with the palatine glands which
empty near the internal nares. Similar ridges are not found
paired in any ranid and, therefore, usually serve as a ready means
of identifying the more ranid-like brevicipitids.

The more specialized brevicipitids have lost their teeth and
all the ventral elements of the shoulder girdle (Fig. 172) save the
coracoids. Their heads and feet may be variously modified for
arboreal or fossorial life. Brevicipitids in the Asiatic, East
Indian, and Malagasy regions seem to have independently
run through a series of structural changes, often parallel in the
three regions. In arranging the genera in subfamilies it is very
difficult to distinguish between groups showing the same grade of

528

THE BIOLOGY OF THE AMPHIBIA

evolution and groups which have descended from a common

ancestor. The present arrange-
ment, although not entirely
satisfactory, will serve to iden-
tify the more conspicuous
groups of genera. Three genera
have been placed in separate
monotypic subfamilies. When
the anatomy of other Brevici-
pitidae becomes better known,
they will probably be grouped
with other genera, but at the
present moment their immedi-
ate relationships are unknown.

Subfamily 1. Dyscophinae.
— Brevicipitids with large, en-
tire prevomers, surrounding the
internal nares except on the
outer side; omosternum, clavi-
cles, procoracoids, and sternum
present. Dyscophus of Mada-
gascar and Calluella of Suma-
tra, India, and southern China
are the most primitive genera.
They agree in having large pre-
vomers with the teeth arranged
in a transverse row behind the
internal nares. The sacrum in
these genera is only slightly
dilated, the omosternum is
small. They possess maxillary
teeth and resemble the.semifos-
sorial species of Rana in general
appearance. From these two
stocks there has arisen in differ-
ent regions a host of genera.
Only three of these derived
genera have diverged so slightly
from the ancestral stocks that
they are grouped in the same subfamily with them.

Fig. 172. — Reduction of the pectoral
girdle in the breviciptid toads. A.
Microhyla pulchra. B. Kaloula ver-
rucosa. C. Kalophrynus pleurostigma.

RELATIONSHIPS AND CLASSIFICATION 529

Callulina, known only from kreffti of Tanganyika Territory, is
a toothless form which retains the large prevomers of Dyscophus.
Its omosternum and sternum are cartilaginous but well developed.
Its sacrum is much expanded and the terminal phalanges are T-
shaped. It represents the primitive brevicipitid stock in Africa.

The two Madagascan genera Pseudohemisus and Scaphio-
phryne are outwardly very different from Dyscophus but they
retain the undivided prevomer of that genus. Maxillary teeth
are lacking in both, and the prevomer forms a posteriorly directed
process which partially overlies the palatine (see Noble and
Parker, 1926). In Pseudohemisus the clavicle is a narrow splint
reaching the scapula and midline of the girdle, while in Scaphio-
phryne it is further reduced and does not reach the midline
The former genus lacks, the latter possesses, digital dilations.
The former includes four species, the latter, only one.

Dyscophus is one of the most distinctive of all Salientia. It
is known from six species, most of which when fully adult are
large and tinged with bright purplish red. This color is very
unusual among Salientia, and it is perhaps not mere coincidence
that Calluella, Calliglutus, and a few other brevicipitids are
similarly tinged, though to a lesser degree. It is interesting to
note that Calluella and Dyscophus are more closely allied to
each other than either is to Callulina. This would seem to afford
evidence of a former Indo-Madagascan connection at some earlier
time (see page 452), whether or not this connection ran via Africa.

Subfamily 2. Rhombophryninae. — Brevicipitidae with the
prevomers of each side divided into two pieces, the posterior
overlying the palatines (apparently replacing it in Anodontohyla
and Stumpffia). The Rhombophryninae are peculiar to Mada-
gascar. They apparently arose from Dyscophus-like ancestors,
although some genera are equipped with very large adhesive finger
discs (Fig. 173) and others have simple toes without pads.
Within this single subfamily confined to a limited area there has
developed arboreal, terrestrial, and fossorial types, none of which
shows a close affinity to genera living on the mainland of Africa
or Asia. That the Rhombophryninae actually represent a single
closely allied group of genera is shown by their palatal bones.
In no other Salientia are the prevomers divided into two parts.
The only other Amphibia which exhibit a similar splitting of the
prevomers are the Plethodontidae, which are obviously a natural
group of genera. The posterior part of the prevomer overlies

530 THE BIOLOGY OF THE AMPHIBIA

the palatine, not the parasphenoid as in the plethodontids. The
teeth on these posterior pre vomers have been called " palatine."
As a matter of fact, true teeth are never found on the palatine
bones of any Salientia.

The genera of Rhombophryninae are best distinguished by
comparing their skull and pectoral girdle elements. Mantipus,
Platyhyla, Platypelis, and Plethodontohyla retain the maxillary
teeth, and their posterior prevomer is a broad transverse plate
overlying the palatines. In Plethodontohyla the clavicles are

Fig. 173. — Brevicipitid toads. The Brevicipitidae exhibit a wide range of
adaptive radiation. Some species, .such as Platyhyla verrucosa (A) of Madagas-
car are arboreal and have large adhesive discs. Many, such as the American
Gastrophryne carolincnsis (B), are fossorial, and have narrow, pointed heads and
rotund bodies.

absent; in the others, present. Mantipus retains the complete
clavicle of Dyscophus, while in Platyhyla and Platypelis it is
reduced and does not reach the scapula. Platyhyla retains a
complete row of vomerine teeth, while in Platypelis the vomerine
teeth are restricted to the mesial end of the posterior prevomer.
The most distinctive genus in this series is Platyhyla, with its
enormous discs and hyla-like appearance (Fig. 173, A).

The remaining genera of Rhombophryninae are more easily
distinguished than the preceding. Rhombophryne is a little
toadlike creature with a peculiar warty face (Fig. 34, B). It

RELATIONSHIPS AND CLASSIFICATION

531

lacks maxillary teeth, but the posterior prevomers bear toothlike
structures on their whole width. The clavicle is lacking and the
procoracoid is reduced to a narrow slip not resting on the cora-
coid. Cophyla is a very small tree frog with large digital dila-
tions. It retains maxillary teeth, but the posterior prevomers are
fused in the midline to form a small dentigerous plate. Anodon-
tohyla and Stumpffia are recognized by their small first (inner)
finger. In both these the clavicles and procoracoids are present
as in Dyscophus, but in Stumpffia the clavicle extends only two-
thirds the length of the procoracoid. Anodontohyla possesses
maxillary teeth, and Stumpffia, which is a very small form, lacks
them. In both Anodontohyla and Stumpffia the prevomer is
small, closely pressed to the mesial side of the internal nares, and
without teeth. This suggests that the posterior part has been
lost or fused to the palatines. Neither genus is closely related to
any other member of the subfamily, and it is perhaps doubtful
if they should be included in the same group with the other genera,
which apparently represent a natural series.

Subfamily 3. Sphenophryninae. — Brevicipitidae with the char-
acters of the Dyscophinae, except that the omosternum is
lacking. The Sphenophryninae range from the Philippines,
Borneo, and the Celebes through New Guinea to northern
Queensland. Two of the four genera are restricted to New
Guinea. The Sphenophryninae were obviously derived from
Dyscophinae and apparently from Calluella, which they approach
closely in structure.

Liophryne of New Guinea seems to be the most primitive. It
approaches Calluella closely in body form. The prevomers have
the same extent as in Calluella but the vomerine teeth of the latter
are replaced by a single row of small odontoids. Maxillary teeth
are absent.

The other genera in the subfamily were described as lacking
the vomerine teeth. All, however, have a sharp, crenulated ridge
across the posterior edge of the prevomers. In some species of
Sphenophryne the ridge is lacking, but in others it simulates a
row of small teeth. Sphenophryne is identical to Liophryne
except that it lacks the vomerine odontoids and usually has larger
digital dilations. The large L. rhododactyla, however, has a large
calcified omosternum. Oxydactyla, known from a species con-
fined to New Guinea, is a Sphenophryne without digital dilations,
the terminal phalanges being simple. Oreophryne is merely a

532

THE BIOLOGY OF THE AMPHIBIA

Sphenophryne with clavicles tilted at a sharp angle to the cora-
coids and not reaching the scapulae.

It is interesting to note that a modification of the clavicles,
identical to that of Oreophryne, has occurred in a very dif-
ferent stock of brevicipitids. The South American Chiasmocleis
differs from Hypopachus of the same region by its short procora-
coids and clavicles set at an angle to the coracoids as in the case of
Oreophryne.

Sphenophryne and Oreophryne represent the dominant brevi-
cipitids of the East Indies. Each is represented by 10 or 12
species. Some species of Oreophryne practice direct develop-
ment (as in the case of all East Indian brevicipitids, as far as
known), but one species of Sphenophryne is said to pass through
the tadpole stage.

Subfamily 4. Cacopinae. — Brevicipitids with the prevomers
surrounding the internal nares as in the Dyscophinae; the
omosternum, clavicles, and procoracoids (except in Colpoglossus)
absent. The Cacopinae seem to have arisen partly in the East
Indies from the Sphenophryninae and partly in southern Asia
from Dyscophinae. They have a broad distribution throughout
southern Asia and the Indo- Australian Archipelago.

The most primitive genus of Cacopinae seems to be Colpog-
lossus, of Borneo. It retains true teeth on the maxillaries and in a
long row across the prevomers as in Calluella and Dyscophus.
The digits are without discs but the terminal phalanges are bluntly
T-shaped. The sacrum is only slightly dilated. The body form
is depressed as in Calluella. The pectoral girdle is more primi-
tive than in other Cacopinae, for a distinct rudiment of the pro-
coracoid cartilage is retained. Colpoglossus is specialized in
that the posterior part of the tongue is tightly bound to the mid-
dle of the floor of the mouth. This makes the posterior edges of
the tongue curl over to form a shallow pocket. In Glyphoglossus
among the Cacopinae and in many other subfamilies of brevici-
pitids, a parallel modification has occurred, except that in these
the whole median portion of the tongue is usually tightly fixed,
producing a crease for the greater part of its length (Fig. 174).

Calliglutus of Borneo is apparently identical to Colpoglos-
sus, except that the tongue is not creased and the body is less
depressed.

The two burrowing toads of India, Cacopus and Glyphoglossus,
are closely related. The maxillaries are toothless and the pre-

RELATIONSHIPS AND CLASSIFICATION

533

vomers are very similar in the two forms. In Glyphoglossus the
prevomers are studded with two or three bony swellings of which
the posterior mesial ones form a pair of rounded projections. In
Cacopus these same processes are present but longer and pointed.
In life they are covered with pigmented mucosa. The palates
are otherwise identical in the two genera. The chief difference
between Glyphoglossus and Cacopus lies in the tongue, which is
modified in the former as in Colpoglossus except that the pocket
extends forward as a median groove or fold to the anterior part
of the tongue. As already pointed out, this is a modification
which has cropped up many times in the Brevicipitidae.

Fig. 174. — Head of Glyphoglossus molossus, showing the grooved tongue charac-
teristic of various brevicipitids.

The remaining genera of Cacopinae seem very closely related.
The widespread Phrynomantis (Hylophorbus of authors) appears
to be the central type. It ranges from the Philippines to New
Guinea and Australia. It has a crenulated ridge across the
posterior margins of the large prevomers. The usual soft ridges
across the back of the roof of the mouth are present. It has
digital dilations, T-shaped terminal phalanges, but no webs.

Copiula of New Guinea differs from Phrynomantis in its slightly
more pointed head and in lacking the anterior of the two soft-
palatal ridges. This is hardly a generic difference in view of the
extreme variability of the ridge in many other brevicipitids.
Cophixalus, of New Guinea, has a palate similar to Copiula but
its toes are slightly webbed. Here, again, the question is raised
of whether this can be considered a generic difference. Both
genera are represented by only a single species (possibly two in
Copiula). If these forms were not rare species coming from a

534

THE BIOLOGY OF THE AMPHIBIA

little known country, they probably never would be considered
types of distinct genera.

Choerophryne, also known from only a single New Guinean
species, may be considered a Phrynomantis with a long, pointed
snout and with large discs. Its prevomers are, however, firmly
fused to the ethmoid and lack transverse ridges. Aphantophryne
is another monotypic genus from New Guinea. It has a small,
round head and no digital discs. Nevertheless, it retains the
T-shaped terminal phalanges and seems to differ from Phryno-
mantis chiefly in the reduced pectoral girdle. The sternum,
according to Fry, is entirely absent.

Genyophryne, the last genus in the subfamily, was at one time
considered the type of a distinct family, and Van Kampen (1923)
retains it as representing a distinct subfamily. A careful
inspection of its anatomy will show, however, that it is closely
allied to Phrynomantis. It differs chiefly in its prevomers, which
bear a patch of odontoids on their mesial half. The extreme
anterior margins of the dentaries are slightly crenulated, suggest-
ing a small series of very small teeth. A similar, but more exten-
sive, modification occurs in Megaelosia, and, as pointed out
above, many genera of frogs have their dentaries extended into
a more pronounced sawtooth edge than Genyophryne. It is
possible that Genyophryne was derived from a more Calluella-
like frog than Phrynomantis. Its head and body are much
depressed. Its sacral diapophyses are only moderately dilated.
The toes are slightly webbed. Genyophryne agrees with a few
other brevicipitids in reverting to a procoelous vertebral column.
The bones of the skull are partly involved in a secondary ossifica-
tion, although this does not include the derm. The mandibles,
squamosals, and frontoparietals are studded with this bony
deposit and extended in width. In other families of frogs a
secondary deposition of bone on the skull usually brings with it
the formation of odontoids on the prevomers or palatines. The
same seems to be the case in Genyophryne, which differs from
Phrynomantis chiefly in those parts affected by this secondary
deposit.

Subfamily 5. Symphygnathinae. — Brevicipitids restricted to
New Guinea and differing from all other Salientia in that the
maxillaries are extended forward and meet in symphysis anterior
to the premaxillaries; in other characters agreeing closely with
the Cacopinae. There can be very little hesitation in pro-

RELATIONSHIPS AND CLASSIFICATION 535

nouncing the five genera included in this subfamily as closely
related, for no other Amphibia exhibit the same type of skull
modification. Further, these genera have the same reduced
pectoral girdle, and their prevomers extend posterior to the inter-
nal nares as a broad plate on each side.

The most primitive genus in the series appears to be the large
Callulops. As this genus has been incorrectly defined in most
previous texts, it may be described in full: pupil probably hori-
zontal; tongue large, completely attached behind; prevomers
large, extending around the choanae and forming a ridge provided
with a row of small odontoids transverse to the body axis; a soft,
denticulated ridge between the oesophagus and buccal cavity ; a
narrow, smooth ridge anterior to this and extending almost
across the roof of the mouth as a widely open crescent ; tympanum
distinct; fingers and toes free, the tips with small discs; outer
metatarsals united; no procoracoid or clavicle; terminal phalanges
T-shaped.

Mantophryne is identical to Callulops but lacks the odontoids
on the prevomer ridges. This is again a character hardly of
generic value, especially as the odontoids tend to be lost in dried
skeletons of Callulops. Xenobatrachus seems to have arisen
directly from Callulops in another direction. Its tongue is more
firmly attached and bears a deep median groove, as in Glypho-
glossus and Ctenophryne. At least this is the case in rostratus,
bidens, and giganteus. In macrops it is intermediate between
this condition and that in Callulops. In all these species of
Xenobatrachus the posterior mesial margin of each prevomer is
raised into one or two prominant spikes which may or may not
pierce the mucosa. This is apparently a parallel modification to
that in Cacopus but does not indicate very close affinity. The
name Xenorhina is reserved for a single species of Xenobatrachus
which lacks the prevomer spikes. Its tongue is grooved, as in
most species of Xenobatrachus. Here, again, it is merely a
matter of opinion whether the name should be recognized.

The fifth genus in the subfamily has been placed in at least
three different families by different authors, who apparently made
little attempt to investigate its anatomy. The only species of
Asterophrys is a depressed frog similar to Genyophryne. Its
head is not involved in cranial ossification, but a sagittal crest,
apparently a secondary sheet of bone, separates the two masses
of temporal muscles which completely cover the frontoparietals.

536

THE BIOLOGY OF THE AMPHIBIA

It possesses a long, crenulated ridge across the posterior edge of
each prevomer. These lack odontoids and therefore resemble
those of Mantophryne. Its tongue is firmly attached only toward
the rear and thus forms a pocket, as in Colpoglossus and in Man-
tophryne macrops. The terminal phalanges are T-shaped, but
the digital dilations are small.

The best evidence of its relationships is to be seen in its rostrum,
which exhibits an overlapping of the maxillaries on the premaxil-
laries as in the other genera in the subfamily.

Subfamily 6. Kalophryninae. — Brevicipitidae in which the
prevomers are small and restricted to the anterior and mesial
margins of the choanae; procoracoids and clavicles present, but
the omosternum reduced or absent, the usual pair of ridges on the
posterior part of the palate. The Kalophryninae were appar-
ently derived directly from Calluella or at least from the Dysco-
phinae. Only one genus, Kalophrynus, is found today in Asia,
the other five are American. Still this genus has a broad distribu-
tion from Sumatra and the Malay Peninsula across Borneo and
Southern China to Hainan and the Philippines.

Kalophrynus is the most primitive type. It differs from Cal-
luella in its reduced prevomers and toothless maxillaries. It has
also a narrower head and smaller mouth. Although Kalophrynus
was derived from a type close to Calluella, it has stronger and
straighter procoracoids and clavicles than in that genus.

The American Hypopachus is extremely close to Kalophrynus
in structure. Its prevomers are slightly more reduced. The
pads just posterior to the internal nares of Kalophrynus, and
forming such a characteristic feature of this genus and Kaloula,
are lacking. Further, the pupil is erect instead of horizontal.
Hypopachus is distributed from Paraguay to the United States.

Otophryne of British Guiana is probably not generically distinct
from Hypopachus. It is a large, square-headed frog. It is
supposed to be distinguished from Hypopachus by its distinct
tympanum and round pupil. Neither of these characters in
other groups is always of generic value.

Chiasmocleis and Nectodactylus parallel Oreophryne and
Platyhyla in the reduction and tilting of the procoracoid and
clavicle. These genera come from Paraguay and Brazil, respec-
tively. Except for their short procoracoid and clavicle, which
do not reach the scapula and are directed partly forward, they
approach closely to Hypopachus in structure. The genera are

RELATIONSHIPS AND CLASSIFICATION 537

each known from only a single species. Nectodactylus differs
from Chiasmocleis in its short, webbed fingers. The webs are
very fleshy and give the hands the appearance of being thrust into
bags.

The last genus, Stereocyclops, is not well known. It is sup-
posed to differ from Hypopachus chiefly in having the sclerotic
membrane ossified to form an annulus around the eye. The type
in the Museum of Comparative Zoology shows that this annulus
is merely a feeble development of dermal ossification both over
the eyes and over the snout. The genus should not be separated
from Hypopachus.

Subfamily 7. Microhylinae. — Brevicipitidae with the reduced
prevomers of the Kalophryninae but no clavicle or procoracoid
present (except in Gastrophrynoides) . The Microhylinae were
apparently derived from the Kalophryninae. Three genera are
found in southeastern Asia, including the western part of the
Malay Archipelago, and three others in the Americas.

Microhyla, which has an extensive range in southeastern Asia
and adjoining islands, seems to be the most primitive genus. It
differs from Kalophrynus in its reduced pectoral girdle, circular
pupil, and smooth anterior palate.

Phrynella, from the Malay region, Sumatra, and Borneo, is
apparently closely related to Microhyla. Its toes are cylindrical
but its fingers are broadly dilated. Its subarticular tubercles
(Fig. 162) are enormous and apparently assist it in its tree-
climbiDg habits. As in Microhyla, there is no procoracoid or
clavicle but a rudiment of an omosternum. Phrynella is known
from two species.

Gastrophryne is perhaps not generically distinct from Micro-
hyla. Most species of the latter are long-limbed forest frogs,
very different from the semifossorial, narrow-mouthed toads of
the United States. Some species of Microhyla, such as rubra of
Ceylon, are practically identical to certain species of Gastro-
phryne as elegans of Mexico. Gastrophryne is supposed to
differ in its webless toes, but certain species of Gastrophryne, as
aterrimum, possess webs. It must be admitted that there is no
generic difference between Microhyla and Gastrophryne, and if
the former name is retained it can be only on the general appear-
ance of the greater number of species.

Ctenophryne of Colombia is one of the more webbed species of
Gastrophryne having an adherent grooved tongue as in Gly-

538

THE BIOLOGY OF THE AMPHIBIA

phoglossus, Xenobatrachus, etc. It is known only from a single
species. The sudden appearance of this tongue modification in
the American Brevicipitidae is further evidence of the haphazard
nature of its occurrence.

The recently described Dasypops of Brazil is merely a Gastro-
phryne with the scapula articulated with the base of the skull.
A parallel modification occurs in the African Hemisus. Gastro-
phrynoides of Borneo appears to be a Microhyla with a thin
cartilaginous procoracoid.

Subfamily 8. Phrynomerinae. — Brevicipitidae without pro-
coracoid or clavicle; an intercalary cartilage present between the
last two phalanges of each digit. The African Phrynomerus is
not closely related to any other brevicipitid. It has, therefore,
been made the type of a distinct subfamily. Its most peculiar
features are its intercalary cartilages, which are not found in any
other brevicipitid. Its sacral diapophyses are greatly dilated,
its prevomers are small. Phrynomerus is known from five species
which are widely scattered over Africa south of the Sahara.

Subfamily 9. Kaloulinae. — Brevicipitids lacking maxillary
teeth and clavicles but retaining an omosternum and a rudiment
of the procoracoids attached to the coracoids near the midline.
Kaloula is the most primitive genus in this small subfamily. It
has a wide distribution throughout eastern Asia as far north as
Manchuria and as far west as the western part of the Malay
Archipelago. It retains large prevomers extending posterior to
the internal nares. The posterior edge of these prevomers is
raised into a sharp, often crenulated, edge which is covered in
life with mucosa. Ramanella, of India, is a small form of Kaloula
which has reduced the prevomers to small bones which do not
extend posterior to the internal nares. The fingers of both
Kaloula and Ramanella are often dilated, the terminal phalanges
T-shaped.

Subfamily 10. Melanobatrachinae. — Brevicipitids with a cal-
cified omosternum, clavicle, and procoracoid present; the pre-
vomers small, reduced to a pair of splints mesial to the internal
nares; palate without ridges. The little black toad of India,
Melanobatrachus, is unquestionably a primitive brevicipitid, as
shown by its very complete pectoral girdle. But it shows no
close affinity to the primitive Dyscophinae of Asia. Its squarish
head, coal-black color, and rough skin give it the appearance of
Dendrophryniscus stelzneri of Brazil, a representative of a very

RELATIONSHIPS AND CLASSIFICATION

539

different family. It is possible that it is related to the Madagas-
can Dyscophinae with reduced pre vomers (Stumpffia), but our
knowledge of these is very fragmentary.

Melanobatrachus is known from only a single species. This
species probably lays its eggs in the water. A female 31 mm.
long had densely pigmented eggs 2 mm. in diameter. Melano-
batrachus feeds on termites, beetles, and worms.

Subfamily 11. Brevicipitinae. — Brevicipitidae with the roof
of the mouth very glandular, either a broad, porous gland cover-
ing nearly the entire roof of the mouth or several pairs of glan-
dular folds between internal nares and oesophagus. The African
Breviceps and Spelaeophryne are of uncertain affinities. Brevi-
ceps includes six or more short-headed, burrowing toads. They
retain clavicle and procoracoid without an omosternum or with
a very much reduced cartilaginous one. The sacrum and coccyx
are fused as well as the first and second vertebrae.

Spelaeophryne is known only from the type. It differs from
Breviceps in its slimmer form, free coccyx, and different palate.
A clavicle and procoracoid, although broken in the type specimen,
are present and very similar to those of Breviceps.

The little African Didynamipus may be referred provisionally
to this subfamily. It retains the pectoral girdle of Breviceps,
but its palate is unknown. It parallels Breviceps in the reduc-
tion of its lateral digits. Didynamipus is, however, a forest frog,
known only from the Cameroons and Fernando Po.

Callulina should probably be referred to this subfamily instead
of to the Dyscophinae. It has an additional ridge across the
palate which is apparently glandular. The Brevicipitinae
although often of grotesque appearance retain many of the
primitive skeletal characters of the Dyscophinae.

Subfamily 12. Hoplophryninae. Small East African toads
differing from all other African brevicipitids in the great reduc-
tion of the first (inner) finger.

The two genera in the subfamily are closely related and may
have descended from Callulina for Parhoplophryne, the more
primitive genus, retains a narrow but complete clavicle. In
Hoplophryne the clavicle is reduced to a nodule. The reduced pre-
vomers of both genera do not extend posterior to the choanae, and
this represents a further divergence from the primitive condition.
The eggs of Hoplophryne are laid between the leaves of banana
plants or in old bamboo stems, but the larvae which hatch under

540

THE BIOLOGY OF THE AMPHIBIA

these cramped conditions agree essentially with other brevicipitid
larvae.

Subfamily 13. Hemisinae. — Brevicipitids with a very pointed
snout, the procoracoid and clavicle present, and the pectoral
girdle articulating with the skull. The African Hemisus is of
uncertain affinities and has been isolated provisionally in a
separate subfamily. It is possibly related to Breviceps, but its
palate lacks the large glands of that genus. Its eggs, although
laid on land, develop into tadpoles of a ranid type. This strongly
suggests that Hemisus has arisen independently from ranids and
has no close affinity to the other Brevicipitidae. Hemisus has a
wide distribution throughout the more arid parts of Africa. It is,
however, represented by only two species.

Subfamily 14. Cacosterninae. — Small African brevicipitids,
usually with maxillary teeth, no clavicle, the procoracoid either
present or rudimentary, the omosternum bony or cartilaginous;
no ridges or glandular swellings on the palate, terminal phalanges
either simple or knobbed. The Cacosterninae have probably
directly evolved from small African ranids, Arthroleptinae.
This is suggested by the life history (see page 64), the tadpole
being of the Rana type instead of similar to that of other brevi-
cipitids (Noble, 19266). Cacosternum is known from two or
three species, one of which, closely related to the others, lacks
maxillary teeth. Anhydrophryne is represented by a single
South African species. Both Cacosternum and Anhydrophryne
resemble Arthroleptis closely. Cacosternum has a more dilated
sacrum and a more reduced pectoral girdle than Anhydrophryne
has.

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Physalaemus, and Pleurodema, Ann. Mag. Nat. Hist. (9), XX, 450-478.

Homer, A. S., 1930: The Pennsylvanian tetrapods of Linton, Ohio, Bull
Amer. Mus. Nat. Hist., LIX, 77-147.

Sollas, W. J., 1920: On the structure of Lysorophus as exposed by serial
sections, Phil. Trans. Roy. Soc. London., Ser. B, CCIX, 481-527.

Van Kampen, P. N., 1923: "The Amphibia of the Indo-Australian Archi-
pelago," Leiden.

Vidal, L. M., 1902: Sobre la presencia del tramo Kimeridgense en el Mont-
sech (Lerida) y hallazgo de un batracio en sus hiladas, Mem. R. Acad.
Cienc. Artes Barcelona (3), IV, No. 18, 263-267.

542

THE BIOLOGY OF THE AMPHIBIA

Watson, D. M. S., 1919: The structure, evolution and origin of the

Amphibia — the "orders" Rachitomi and Stereospondyli, Phil. Trans.

Roy. Soc. London, Ser. B, CCIX, 1-73.
, 1926: The evolution and origin of the Amphibia, Phil. Trans. Roy.

Soc. London, Ser. B, CCXIV, 189-257.
, 1926a: The Carboniferous Amphibia of Scotland, Palaeontologica

Hungarica, I, 221-252, 3 pis.
Whittard, W. F., 1930: The structure of Branchiosaurus flagrifer, sp.n.

and further note on Branchiosaurus amblystomus, Credner, Ann. Mag.

Nat. Hist. (10) V, 500-513.

Comprehensive Taxonomic Works

General:

Boulenger, G. A., 1882: "Catalogue of the Batrachia Gradientia S.

Caudata and Batrachia Apoda in the Collection of the British

Museum, " 2d ed., London.
, 1882: "Catalogue of the Batrachia Salientia S. Ecaudata in the

Collection of the British Museum," 2d ed., London.

, 1910: "Les Batraciens et Principalment Ceux d'Europe," Paris.

Nieden, F., 1913: Gymnophiona (Amphibia Apoda), Das Tierreich, Lief.

37, Berlin.

, 1923: Anura I, Subordo Aglossa und Phaneroglossa, Sectio I

Arcifera, Das Tierreich, Lief. 46, Berlin and Leipzig.

, 1926: Anura II, Engystomatidae, Das Tierreich, Lief. 49, Berlin

and Leipzig.

North America:

Cope, E. D., The Batrachia of North America, Bull. U. S. Nat. Mus. 34.
Dickerson, Mary C, 1906: "The Frog Book; North American Frogs and

Toads, with a Study of the Habits and Life-Histories of Those of

the Northeastern States," New York.
Dunn, E. R., 1926: "The Salamanders of the Family Plethodontidae,"

Northampton, Mass.
Hay, Oliver P., 1892: The batrachians and reptiles of the State of

Indiana, Ind. Dept. Geol. and Nat. Resources Ann. Rept., 1891, 401-

602.

Hurter, Julius, Sr., 1911: "Herpetology of Missouri," St. Louis, Mo.
Jordan, David Starr, 1929: "Manual of the Vertebrate Animals of the

Northeastern United States," New York.
Pratt, H. S., 1923: "A Manual of Land and Fresh Water Vertebrate

Animals of the United States," Philadelphia.
Ruthven, A. G., Crystal Thompson, and Helen T. Gaige, 1928: The

herpetology of Michigan, Mich. Handb., Ser. 3.
Slevin, J. R., 1928: The amphibians of Western North America, Occ.

Papers Cal. Acad. Set., XVI.
Stejneger, L., and T. Barbour, 1923: "A Check List of North American

Amphibians and Reptiles," 2d ed., Cambridge.
Strecker, J. K., 1915: Reptiles and amphibians of Texas, Baylor Bull.

XVIII, No. 4.

RELATIONSHIPS AND CLASSIFICATION

543

South America:

Miranda-Ribeiro, Alipio de, 1926: Notas para servirem ao estudo dos
Gymnobatrachios (Anura) Brasileiros, Arch. Mus. Nacion. Rio de
Janeiro, XXVII.

West Indies:

Barbour, T., 1914: A contribution to the herpetology of the West

Indies, Mem. Mus. Corny. ZooL, Cambridge, Mass., XLIV, No. 2.
Barbour, T., and C. T. Ramsden, 1919: The herpetology of Cuba, Mem.

Mus. Corny. ZooL, Cambridge, Mass., XL VII, No. 2.
Schmidt, K. P., 1928: Amphibians and land reptiles of Porto Rico,

Scientific Survey of Porto Rico and the Virgin Islands, X, Part I,

N. Y. Acad. Sci.

Stejneger, L., 1904: The herpetology of Porto Rico, Ann. Rey. U. S.
Nat. Mus., 1902.

Euroye:

Boulenger, G. A., 1897: "The Tailless Batrachians of Europe," Parts

1-2, London, Ray Soc.
Nikolsky, A. M., 1918: "Faune de la Russie; Amphibiens," Petrograd.
Schreiber, Egid., 1912: " Herpetologia Europaea," Jena.

Africa:

Noble, G. K., 1924: Contributions to the herpetology of the Belgian
Congo based on the collection of the American Museum Congo
expedition 1909-15, Bull. Amer. Mus. Nat. Hist., XLIX, 147-347.

Asia:

Boulenger, G. A., 1890: "Reptilia and Batrachia; The Fauna of British

India including Ceylon and Burma," London.
, 1912: "Reptilia and Batrachia; A vertebrate fauna of the Malay

Peninsula," London.
, 1920: A monograph of the South Asian, Papuan, Melanesian and

Australian frogs of the genus Rana, Rec. Ind. Mus., XX, 1-226.
Dunn, E. R., 1923: The salamanders of the family Hynobiidae, Proc.

Amer. Acad. Arts. Sci., LVIII, 445-523.
Smith, M. A., 1930: The Reptilia and Amphibia of the Malay Peninsula,

Bull. Raffles Mus., Singapore, No. 3.
Stejneger, L., 1907: The herpetology of Japan and adjacent territory,

Bull. U. S. Nat. Mus. 58.

East Indies:

Van Kampen, P. N., 1923: "The Amphibia of the Indo- Australian Archi-
pelago," Leiden.

INDEX

Bold face type indicates pages w.
more important discussions appear.

Abbott, 420
Abdominal glands, 113
Abdominal muscles, 110
Abdominohyoideus, 254
Abducens, 362, 367
Abel, 463

Abel and Macht, 134, 135
Absorption and assimilation, 207
Acanthostomatidae, 462
Accommodation of eye, 329
Achelomidae, 460
Acousticolateral area, 365
Acris, 80, 95, 115, 438, 508, 510, 526
Acris gryllus, 152, 407, 409, 420
Acris gryllus crepitans, 407
Acromio-cleido-episterno-humeralis,
258

Acrosome, 15, 18
Actinodontidae, 460
Activation of egg, 17, 40
Adams and Hankinson, 457
Adams and Rae, 281
Adams and Richards, 140
Adams, Richards, and Kuder, 140
Adaptation, 93

and speciation, 79-108
Adaptive value of color differences,
87

Addair and Chidester, 310
Adductor mandibulae, 264
Adelmann, 32
Adelospondyli, 11, 462
Adelotus, 415, 498
Adhesive discs, 64, 79
Adhesive organs, 23, 24, 101
Adolph, 141, 271, 437

illustrations, section headings, or

Adolph and Collins, 140
Adrenal organs, 146, 302
Adrenalin, 135, 195, 304
Aelurophryne, 493
Agafonow, 309
Agalychnis, 513
Age, and area, 452

determination, 444
Aglossal toads, 489, 495
Aglyptodactylus, 525, 526
Aistopoda, 11, 463
Albinism, 82, 148, 149
Alisphenoid, 219
Alkaloids, 135
Allantoic placenta, 55
Allantois, 2, 13, 23, 76
Allen, 293, 298, 300, 301, 307
Allen and McCord, 310
Allen, Torreblanca, and Benjamin,
299

Allen and Wright, 386
Allophores, 143
Allophryne, 510
Altirana, 520
Alveoli, 166

Alytes, 131, 220, 273, 275, 276, 381,
489

Alytes cisternasii, 489
Alytes obstetricans, 409, 489
Ambystoma, 32, 48, 51, 52, 82, 86,
98, 145, 148, 150, 152, 184, 185,
194, 215, 243, 272, 278, 284,
295, 296, 307, 309, 318, 319,
337, 362-364, 368, 371, 378,
379, 382, 387, 388, 414, 417,
419, 423, 424, 434, 43/, 442,
456, 472, 473, 482
common species of, 471

546

THE BIOLOGY OF THE AMPHIBIA

Ambystoma, development of reflexes
in, 378

Ambystoma annulatum, 51, 152

Ambystoma jeffersonianum, 51, 84,
85, 152, 153, 387

Ambystoma maculatum, 28, 29, 33,
35, 51, 84, 85, 143, 152, 194,
344, 371, 386, 387, 400, 419, 435

Ambystoma opacum, 51, 58, 131, 152,
242, 472

Ambystoma tezanum, 152

Ambystoma tigrinum, 28, 29, 33, 35,
51, 52, 152, 194, 295, 368, 434,
435, 437, 444

Ambystomidae, 51-52, 138, 167,
225, 466, 472-473

Ambystomoidea, 465, 471-472, 473

Amino-acids, 207

Amnion, 2, 13, 23, 76

Amniota, 222, 329

Amphibia, defined, 1

Amphicoela, 485

Amphignathodon, 60, 509

Amphiuma, 55, 97, 102, 103, 162,
1.69, 180, 192, 226, 231, 233,
244, 268, 276, 280, 308, 325,
326, 335, 364, 410, 417, 423,
444, 463, 473, 476, 477

Amphiumidae, 55, 476, 477

Amphodus, 125, 511

Amplexus, 242

Ampulla, 336

Amygdaloid, 358

Amylase, 207

Anamnia, 266, 362

Anconeus, 259

Andrias, 469

Aneides, 57, 58, 95, 125, 414, 416,

417, 423, 482
Aneides aeneus, 58, 87, 125
Aneides flavipunctatus, 153
Aneides lugubris, 58, 125, 173, 182,

410, 413, 454
Angular bone, 213
Anhydrophryne, 64, 540
Anomocoela, 491-492, 495
Anondontohyla, 529, 531
Anterior lobe of pituitary, 35, 140
Anthony and Vallois, 258

Anthracosauridae, 460
Anton, 325
Anura, 485

Aorta, 185, 187, 189, 195
Aortic arches, 185
Aphantophryne, 534
Applerot, 111
Aqueous humor, 331
Archegosauridae, 160, 460
Archenteron, 22
Arcualia, 227, 230
Arey, 331

Arm and shoulder musculature, 256
Armistead and Martin, 304
Aron, 294, 302, 305, 307
Arterioles, 193, 194
Arthroleptella, 515
Arthroleptella lightfooti, 71, 115
Arthroleptides, 520, 521
Arthroleptides martiensseni, 521
Arthroleptinae, 515-516, 540
Arthroleptis, 494, 515, 516 540
Arthroleptis batesii, 515
Arthroleptis stenodactylus, 516
Articular, 220

Articular tubercles, enlargement of,
502

Arytenoids, 170

Ascaphus, 15, 76, 87, 88, 104, 132,
186, 196, 218, 220, 221, 229,
240, 250, 257, 260, 262, 266,
283, 303, 335, 408, 421, 451,
453, 485, 487

Ascher, 149

Asperities, 111

Aspherion, 515

Asterophrys, 535

Astylosterninae, 516-518

Astylosternus, 517

Astylosternus diadematus, 517

Astylosternus robustus, 110, 164,
517, 518

Atelopus, 231, 507, 508

Athanasiu, 434

Atlas-axis complex, 232

Atrium, 189

Atwell, 297, 300

Atwell and Woodworth, 298

Auditory apparatus, 29, 87, 221

INDEX

547

Auditory centers, 3
Auricles, 187, 189-192, 194
Auricular lobes, 364
Autonomic system, 371, 372
Autotomy, 36

Axolotl, 52, 82, 102, 131, 134, 147,
149, 151, 210
albino, 81
gastrulation in, 21
limb development, effect of mal-
nutrition or high tempera-
tures on, 33
regeneration of gills in, 36
Ayyanger, 426

Babak, 150, 171, 209, 293, 400
Babina, 126

Bacillus hydrophillus fuscus, 438

Bacteria, 209

Baglioni, 363, 365

Balancer, 23, 28, 35, 48, 51, 53, 59

Baldwin, 307, 308

Balinsky, 38

Ballowitz, 143

Banta, 149

Banta and Gortner, 148
Banting and Best, 301
Barbels, 164
Barbour and Noble, 507
Barbourula, 489
Barcroft, 179
Barrell, 165
Barrows, 443
Barthelemy, 420
Basibranchial, 30
Basidorsals, 227
Basihyal, 30, 225
Basioccipital, 214
Basioccipital condyles, 213
Basipterygoid processes, 213, 219
Basis cranii, 6, 213
Basisphenoid, 9, 213, 214
Basiventrals, 227
Basophilic leucocytes, 182
Basophilic plasmocytes, 182
Bastert, 175
Bataillon, 18, 41

Batrachia, 1, 485
Batrachia Ecaudata, 485
Batrachia Gradientia, 465
Batrachomyia, 441
Batrachophrynus, 91, 164, 486, 499
Batrachophrynus microphthalmus,
444

Batrachoseps, 57, 58, 97, 126, 127,

181, 182, 405, 482
Batrachoseps attenuatus, 231, 444
Batrachoseps pacificus, 91, 92
Batrachuperus, 466-468
Batrachylodes, 524
Batrachylodes vertebralis, 120
Beaumont, 284
Beddard, 226
Beer, 330

Behavior, learned, 392, 394

metabolism and, 434

patterns, 380

temperature and, 433
Belehradek, 292

Belehradek and Huxley, 296, 300
Bell-shaped gills, 54, 67
Bensley, 202
Bensley and Steen, 270
Berg, 207
Beyer, 181
Bickel, 360
Bidder's organ, 278
Biederman, 345, 396
Biedermann, 134, 145
Bieter and Scott, 193
Bikeles and Zbyszewski, 194
Bile, 207, 208
Bindewald, 360
Bischler, 37
Bishop, 414
Blacher, 294, 300
Bladder, urinary, 276
Blanchard, 407, 414, 444
Blastocoel, 21
Blastodisc, 23
Blastopore, 22, 26
Bles, 64, 131, 400
Blind Salamander, European, 483
Blood, 179, 181
calcium, 182

cells, enucleation of red, 181

548

THE BIOLOGY OF THE AMPHIBIA

Blood cells of frog, 180

circulating, 182

clotting, 40

corpuscles, 179
origin of, 183

platelets, 182

pressure, 193

vessels, 184

viscosity of, 193
Bock, 210

Body, proportions, 127

size, 90, 126

temperature, 431
Bogoljubsky, 36

Bombina, 110, 180, 181, 186, 194,
216, 234, 241, 309, 318, 330,
335, 337, 381, 423, 486, 487
Bombina bombina, 120, 380
Bombina variegata, 111, 120
Bone, marrow, 183

mental, 221

secondary dermal, 125
Bonnamour and Policard, 304
Bony casque, 130
Bony plates, 158
Borborocoetes, 500, 504
Borborocoetes miliarus, 75
Bottazi, 366

Boulenger, 42, 88, 110, 111, 137, 146,

387, 494, 521, 522
Bounoure, 277
Bowen, 19

Brachet, 27, 28, 32, 35
Brachycephalidae, 70, 71, 495, 505,

506, 508, 514, 520
Brachycephalinae, 507, 508
Brachycephalus, 130, 423, 508
Brachyopidae, 461
Brain, 5, 32, 110, 111, 176, 356, 368

formation of, 27

of Necturus, 361

phylogeny of, 367
Brambell, 276
Branchial apparatus, 171
Branchial arches, 30, 101, 103,
160-162, 223

in larvae, 23, 24
Branchial clefts, 102
Branchial pouches, 165

Branchial sac, 71

Branchiosaur, 9, 10, 76, 130, 162,
461, 509

Branchiosauridae, 9, 223, 461, 462
Brandt, 33, 38
Brazil and Vellard, 135
Breder, 404

Breder, Breder, and Redmond, 405

Breeding habits, 402

Breeding rhythm, 85

Breeding site, 402

Breeding temperature factor, 422

Bresca, 305

Breviceps, 539, 540

Breviceps parvus, 71

Brevicipitidae, 62, 64, 69, 101,

152, 162, 197, 202, 236, 237,

258, 505, 514, 527-540
teeth in, 25
Brevicipitinae, 539
Bridges, land, 451
Bronchi, 168-170
Brongniart, 2

Brood pouch of Hylidae, 60
Brooding instinct, 413, 414
Brooks, 419
Brosard and Gley, 305
Brownlee and Cameron, 420
Briicke and Umrath, 196
Brues, 421

Bruner, 171-173, 324, 325

Bruyn and Van Nifterik, 390

Buccal cavity, 171, 172, 174

Buccal respiration, 4

Buccopharyngeal movements of
frogs, 175

Buccopharyngeal respiration, 158,
171, 172

Buddenbrock, 207, 266

Bufo, 41, 73, 74, 112, 141, 166, 171,
181, 184, 202, 273, 276, 278,
282, 298, 299, 330, 332, 342,
343, 381, 383, 395, 406, 424,
433, 454, 456, 494, 499, 501,
503, 504, 514
hybridization in, 41

Bvfo alvarius, 96, 453

Bufo americanus, 80, 112, 340, 407

Bufo boreas halophilus, 444, 454

INDEX

549

Bufo calamita, 340, 384, 391, 393, 395

Bufo canorus, 112, 115, 444

Bufo cognatus, 444, 453

Bufo communis hybridization in, 41

Bufo dunni, 98

Bufo fowleri, 433

Bufo funereus, 112

Bufo jerboa, 502

Bufo marinus, 112, 135, 304

Bufo micronotus, 503

Bufo peltacephalus, 98

Bufo preussi, 503

Bufo punctatus, 120, 454

Bufo regularis, 112, 454

Bufo rosei, 406

i^/o super ciliaris, 454

5u/o terrestris, 407

J5m/o viridis, 41, 42, 113

fiu/o vulgaris, 42, 111-113, 137,

278, 283, 383, 410, 411
Bufogin, 134

Bufonidae, 66, 72, 74, 111, 130, 152,
258, 408, 495, 496, 505, 524

ovoviviparous, 74

toothed, 70
Bufonin, 134
Bufoninae, 498, 501-504
Bufotalin, 134
Burnett, 392
Burns, 278
Burns and Burns, 35
Burr, 30, 340
Busquet, 411
Butler, 418
Buxton, 97
Buytendijk, 393, 395

Cacopinae, 532-534

Cacops, 221, 459

Cacopus, 140, 523, 533, 535

Cacosterninae, 527, 540

Cacosternum, 64, 442, 540

Caedlia tentaculata, 464

Caecilians, 11, 12, 76, 130, 132, 141,

159, 160, 166, 169, 174, 187,

192, 195
gastrulation in, 22

Caecilians, laying of eggs in, 23
Caecum, 205
Calcareous egg, 76
Calcium content, 111
Calcium metabolism, 308
Calliglutus, 529, 532
Calluella, 528, 529, 531, 532, 534,
536

Callulina, 529, 539
Callulina kreffti, 529
Callulops, 535

Calyptocephalus, 320, 496, 499
Cameron, 310, 420, 421
Cameron and Brownlee, 420
Camp, 234
Cannon, 374
Capillaries, 141, 193-195

of skin, 163
Capillary tonus, 301
Capitosauridae, 461
Capitulum, 233
Carbohydrates, 205-208
Carbon dioxide, 158, 159, 174, 207,
208

Carbonic acid, 158
Cardinal veins, 185, 186
Cardioglossa, 515
Carmichael, 380
Carotids, 187, 191
Carpalia, 242, 243, 244
Carpus, evolution of, 241
Cartilage, arytenoid, 169

branchial, 187

coracoid, 237

cricoid, 169

laryngeal, 170, 174, 226

Meckel's, 220
Casque, 97
Castration, 305
Catalysts, 85

Caudalipubofemoralis, 262
Caudalipuboischiotibialis, 262
Cells, goblet, 202

Kupffer, 180

Leydig, 132

phagocytic, 179

red blood, 180
Centrale, 33, 242
Centrolene, 118, 510

550

THE BIOLOGY OF THE AMPHIBIA

Centrolenella, 327, 510
Cerathyla, 509

Ceratobatrachus, 418, 509, 523
Ceratobatrachus guentheri, 23, 64
Ceratohyal, 222

Ceratophrys, 74, 125, 382, 384, 416,
423, 442, 497, 499, 500, 518,
523

Ceratophrys americana, 135
Ceratophrys dorsata, 125, 135, 209,
423

Ceratophrys laevis, 318
Ceratophrys ornata, 416, 418
Cerebellum, 357, 364, 367, 369
Cerebral peduncles, 363
Cerebrospinal fluid, 356
Cestodes, 441
Cilia, 130, 171, 202
Ciliary ganglion, 362
Ciliary muscle of eye, 330
Circulatory system, 179, 200
Chamberlain, 456
Champy, 109, 127, 305, 307
Chapman, 82
Charipper, 319
Chase, 275
Chauchard, 360, 363
Chauvin, 115
Chelotriton, 476
Chemical sense, organs of, 321
Chemodifferentiation, 34
Chemotactic effect, 17
Chiasmocleis, 532, 536, 537
Chievitz, 332
Chin pad, 118, 136
Chioglossa, 387, 474, 476
Chioglossa lusitanica, 476
Chiroleptes, 97, 497, 499, 523
Chiromantis, 67, 112, 524, 525
Choerophryne, 534
Chondrocranium, 212, 219
Choroid plexus, 365
Christensen, 273
Chromaffin, 303

Chromatophores, 141, 143, 145, 146
Chromogen, 148

Chromosome, 15, 18, 35, 36, 41, 108
Chromosome aberrations, 81, 85
Clark, 185

Clark and Clark, 183, 197
Clausen, 104

Clavicles, 208, 236, 257, 258
Claws, 138
Claypole, 183
Cleavage, 21 "

of egg, 21

partial, 21
Cleithrum, 234, 258
Cleland and Johnston, 440
Cloaca, 88, 109, 267, 273, 283, 284
Cloacal glands, 284
Cloacal orifice, 208, 286
Cloacal papillae, 109, 307
Coccygeal vertebrae, 231
Coccyx, 196, 197, 230
Cochran, 343
Cocytinus, 11
Coghill, 378, 379
Cohn, 201
Cole, 344, 354, 419
Cole and Allison, 175
Cole and Dean, 345
Collecting tubules, 275
Collin, 438
Color, 115, 116, 135

change, 143, 144

difference, 115

pattern, 90, 146, 147, 152, 163

significance of, 151

tone regulator, 300

variation of, 80
and diet, 151
Colosteidae, 462
Colosteus, 10

Colpoglossus, 532, 533, 536
Columella, 120, 222

cranii, 219
Condyles, 214
Congo Eel, 476
Conklin, 197
Conraua, 519
Conus, 190

Conus arteriosus, 189, 191
Cope, 243
Copeland, 340, 417
Copenhaver, 194
Cophixalus, 533
Cophophryne, 119

INDEX

551

Cophyla, 531
Copiiila, 533
Copula, 225

Copulatory apparatus, 240
Copulatory organ, 74
Coracobrachialis, 258
Coracoid, 236
Coracoid cartilages, 237
Coracoradialis proprius, 258
Corium, 37, 133
Cornea, 326, 327
Cornua, 225
Cornufer, 523, 524
Cornuferinae, 521, 524
Coronoids, 213
Corpora quadrigemina, 363
Corpus striatum, 369
Cort, 441

Cortex-pallial, 360
Corythomantis, 512
Cott, 426, 455
Cotylosaur reptiles, 76
Courtship, 386, 387

behavior, 384

evolution of, 385
Crane, 271

Cranial nerves, 12, 213, 338, 365
Crew, 108, 279
Cricket frog, 115, 508
Cricotidae, 460
Crinia, 76, 407, 498
Criniinae, 492, 496-498, 499, 501
Crofts, 205
Cronheim, 434

Crossodactylus, 113, 504, 507
Crossodactylus gaudichaudii, 113,
126

Crossopterygians, 5, 110, 160, 165
Cruralis, 262
Cry, pain, 409
sex, 409

Cryptobatrachus, 60, 159, 415, 509
Cryptobatrachus evansi brood pouch,
60

Cryptobranchidae, 48-51, 141, 220,
283, 386, 448, 449, 465-466,
468-470
fertilization in, 16

Cryptobranchus, 48, 54, 103, 162,
163, 176, 192, 252, 262, 281,
293, 294, 325, 327, 358, 416,
421, 423, 439, 443, 451, 477
polyspermy in, 17

Cryptobranchus alleganiensis, 48, 468,
469

Cryptotis, 498

Cryptotis brevis, 498

Ctenophryne, 535, 537

Cuenot, 80, 94

Cummings, 395, 403

Cummins, 400

Cunningham, 127

Cutaneous hypertrophies, 113

Cutaneous respiration, 12, 141, 149,

168, 171, 175
Cutaneous veins, 195
Cuvier, ducts of, 189, 192
Cycloramphus, 75, 119, 120, 499
Cynodont reptiles, 4, 219
Cystignathidae, 496
Cytolysins, 103, 104
Czeloth, 401, 403

Dahne, 408

Darwin, 80, 81, 86, 87, 115, 127
Dasypops, 538
Dauvart, 110

Davenport and Castle, 427
Dawson, 132, 184
Dean and Cole, 345
Death feint, 424
Deckert, 415
Defense, 422

reaction, 382, 383, 424
Deltoides clavicularis, 258
Dempster, 338

Dendrobates, 60, 70, 80, 135, 152,

415, 507
Dendrobatidae, 526
Dendrobatinae, 504, 507
Dendrophryniscus stelzneri, 71, 380,

507, 538
Dennert, 139
Dentary (bone), 213, 220

552

THE BIOLOGY OF THE AMPHIBIA

Dentition, 90

Depressor mandibulae, 263
Dermis, 132, 147
Dermosupraoccipitals, 9
Derotreme, 162

Desmognathus, 10, 55-57, 91, 109,
121, 122, 160, 184, 251, 284,
285, 321, 346, 417, 418, 423,
480

Desmognathus fuscus, 55, 56, 80,

305, 346, 402, 413, 419, 423, 467
Desmognathus fuscus carolinensis,

56, 80, 90, 91, 122, 126, 146,

402, 420, 481
Desmognathus fuscus ochrophaeus,

121, 481
Desmognathus phoca, 56, 126
Desmognathus phoca, larva, 481
Desmognathus quadramaculatus, 56,

121, 122, 417, 480-481
Despax, 53

Detwiler, 33, 38, 249, 331, 365, 370,
371

Detwiler and Carpenter, 371
Detwiler and Lewis, 332
Deutsch, 293
Development, 1

arrested, 99

and heredity, 15-47

mechanics of, 25, 28, 35
de Villiers, 71, 442
Diaglena, 509, 512
Dicamptodon, 51, 52, 417, 472, 473
Dickerson, 409
Didynamipus, 539
Dieckmann, 285
Diet, 437

Digestion, 205, 206
Digestive system, 201, 211
Digestive tract, length of, 209

modifications of, 208
Digital loss, 90
Digital scutes, 90

Digital webbing in tree frog, growth

of, 100
Digits, 241, 244

elongated, 115

webbed, 95
Dimorphism, sexual, 121

Dimorphognathus, 124, 125, 509,515
Dimorphognathus africanus, 116
Diplasiocoela, 505, 514
Diplocaulus, 11, 463
Diplovertebron, 239, 241-243
Dipnoans, 45, 101, 160, 165, 186, 187
Discodeles, 523
Discodeles opisthodon, 64
Discoglossidae, 75, 76, 111, 162, 230,
231, 234, 243, 258, 448, 486-489
Discoglossus, 17, 117, 134, 250, 275,
337, 487, 489

fertilization in, 16

hybridization in, 41
Discontinuous evolution, 126
Discophinae, 531

Discs, adhesive and friction, 95, 138
Dispersal, barriers to, 453
Dissorophidae, 460
Dissorophus, 130, 221
Distribution, geographical, 448

migration routes, 450

peculiarities of, 451

present, 449
Dolk and Postma, 434, 174, 207
Dollo, 5

Dominant senses, 340
Doms, 436

Dorsalis scapulae, 258

Douthitt, 11, 463

Drake, 415

Drastich, 182, 436

Druner, 254, 264

Dubecq, 264

Dubois, 281, 331

Duct, Mullerian, 272, 276, 281

perilymphatic, 337

Wolffian, 269, 272, 273, 276
Ducti Cuvierii, 185
Dunn, 113, 126, 134, 222, 335, 416,

453, 457, 479, 480, 482, 507
Duplications, 39
Durken, 34, 368
Dusky salamander, 55, 56, 121
Dwarfing, speciation by, 99
Dwinasauridae, 460
Dwinasaurus, 13, 160, 223
Dye, 318

INDEX

553

Dyscophinae, 528, 529, 532, 536

538, 539
Dyscophus, 528-532

Ear, 28, 333

capsule, 216, 221

external, 334

functions of, 338

inner, 222, 334, 335

middle, 334

ossicles, 334, 335

tonus reflexes of, 339
Eardrum, 120

formation of, 31
Eckstein and Mangold, 425
Ecological niche, 91
Economic value, 416, 456
Ectoderm, 35, 130-132

transplanting in embryos, 26
Ectopterygoid, 244
Edalorhina, 504
Edgeworth, 159, 166, 264
Egg, 13, 15, 48, 108

on back, 60

capsule, 58, 73, 282

foamy mass, 72

frogs', before fertilization, 19

on land, 70

large yolked, 76

number, 70

rods of, 74

sacs, 51

size, 73

strings of, 73, 74
teeth, 73

in vocal pouch, 71
Eggert, 151
Eimer, 147

Eimer's principle of cpistasy, 100
Ekman, 38, 192

Eleutherodactylus, 64, 70, 72, 73,
97, 112, 134, 267, 401, 408,
453, 499, 500, 506, 510

Eleutherodactylus inoptatus, 61, 96,
409

Eleutherodactylus lenlus, 97

Elosia, 75, 112, 113, 504
Elosiinae, 504

Embolomeri, 5-8, 11, 12, 212, 213,
215, 219, 227, 232, 234, 237,
239, 242, 243

Embryo, 130

Eminentia septalis, 358

Emmel, 182

Endocrine glands, 290-316
Endolymph, 337
Endolymphatic sac, 337
Enemies, 442

Energy consumption, surface law
of, 434

Ensatina, 58, 405, 416, 426, 482
Ensatina eschscholtzii, 423
Enucleation, 181
Environment, 75, 128, 395
effect of, 435

relation of Amphibia to their,
431-447

Enzyme, 19, 21, 28, 206, 207

Eobatrachus, 485

Eogyrinus, 6, 221, 334

Eosinophiles, 183

Epaxial muscle mass, 249, 250

Epibranchials, 226, 249

Epidermis, 95, 132, 138, 147, 168

cornification of, 138

vascularization of, 141
Epigenesis, 28-31
Epipterygoid, 219, 244
Episterno-cleido-humeralis longus,
257

Epithalamus, 362
Equilibrium, organ of, 338
Erepsin, 207
Eryopidae, 460

Eryops, 221, 241, 243, 460, 461
Erythrocytes, 179-182, 184, 197
Escher, 53, 318-321
Eugyrinus, 9
Eupemphix, 72, 496, 504
Euproctus, 52, 53, 114, 175, 388,
475

Euproctus asper, 52, 114, 454
Euproctus montanus, 114

554

THE BIOLOGY OF THE AMPHIBIA

Eurycea, 55-58, 59, 91, 102, 123-
127, 146, 152, 160, 284, 285,
357, 389, 390, 423, 479-483
cleavage in, 21

Eurycea bislineata, 57, 98, 102,
123, 148, 292, 299, 389, 419,
479

Eurycea bislineata cirrigera, 479
Eurycea lucifuga, 344, 478
Eurycea multiplicata, 98, 118, 421
Eustachian tubes, 159, 216, 223,
335

Eusthenopteron, 227
Evaporation, rates of, 422
Evolution, discontinuous, 126

divergent, 88

hormones in, 98

parallel, 66, 88, 89, 118

of skull, 214

space and time in, 85

of spermatheca, 285
Excretory system, 266
Exoccipitals, 215
Extensor muscles, 259
External ear, 12

External fertilization, 15, 48, 87
External gills, 57, 73, 76, 171
External nares, 62, 172

in frog embryos, 23
External respiration, 158
Exteroceptive tracts, 358
Eycleshymer, 40, 147
Eyelids, 102, 118, 327
Eyes, 3, 28, 29, 32, 102, 111, 146,
175, 326

of cave salamander, 94

degeneration of, 333

development of, 327

effect of removal of, on brain of
tadpole, 34

in frog embryo, 23

influence of light on, 94

in larvae, 25

median, 309

muscles of accommodation, 330
transplantation of, 29

Faces, toad, 96
Facialis, 263
Faris, 148

Fat bodies, 208, 280, 281
Fat reserve, 206
Faust, 134
Federici, 185
Feeding habits, 415
Fenestra hypoglossal, 213
Fenestra ovalis, 221
Fernandez, 71, 72, 380
Fertilization, 15-21, 48, 49, 109,
283, 387

internal, 15

reaction, 19
Fiber tracts, 34

in brain of frog, 369
Fibrin, 182
Fibrinogen, 182
Fibula, 114, 243
Fibulare, 242, 243
Field, 276
Filatow, 38

Fins, 3, 48, 61, 65, 66, 69, 102
Fischer, 339

Fish, comparison with, 132

Fisher, 81, 112

Flask cells, 140

Fleissig, 326

Fletcher, 76

Flexor muscles, 259

Flower, 394

Flukes, 441

Flying Frog, 426

Foam nest, 66-68, 72

Food, 179, 205

fat as, 205

habits, 70
Foot, skeleton of Rhinophrynus
dorsalis, 79

toad's, regenerative capacity in, 39
Forebrain, 357, 369
Forelimbs, 71, 101, 103, 110, 111

in frog tadpoles, 25, 30

muscles, 255, 263

sexual dimorphism of, 110
Fortuyn, 365

INDEX

555

Four-toed salamander, 58, 92
Fovea, 332

Franz, 99, 101, 328, 344, 345, 391,

393, 395, 404
Frase, 181

Free nerve endings, 321
Friction pads, 135, 521
Frontal, 215

Frontal enlargements, 127
Fuhrmann, 166
Fulton and Huxley, 301
Function, 93

of heart, 193

influence of, 34, 36, 38

of kidney, 270

in phylogeny, 91
Functional stimulus, 34
Functions, sense organs and their,

317-352
Funnel mouth, 69, 70

Gadow, 95, 135, 444, 465
Gall bladder, 205
Gamble, 232, 233
Gampsosteonyx, 517
Gampsosteonyx batesi, 91
Ganoids, 4, 5
Garman, 415
Garstang, 101, 102
Garten and Sulze, 433
Gasco, 386, 387
Gastrocentrophori, 463
Gastrophryne, 62, 101, 537, 538
Gastrophryne aterimum, 537
Gastrophryne carolinensis larvae,

head structures of, 24
Gastrophryne elegans, 537
Gastrophrynoides, 537, 538
Gastrotheca, 54, 60, 137, 160, 408,

415, 423, 509, 510
Gastrothecinae, 67
Gastrulation, 21-23, 26, 28
Gaule, 110

Gaupp, 172, 254, 259, 362
Gayda, 296
Geinitz, 26, 27

Gene mutations, 83, 85, 93, 121, 127,
128

Genes, 19, 21, 82, 83, 86, 88, 101,
102, 109, 127, 128

recessive, 82

recombination of, 181
Genetic factors, 98
Geniohyoideus, 254
Genyophryne, 534, 535
Geobatrachus, 507
Geographic distribution, 448-458
Geotropic response, 401
Gephyromantis, 526
Gessard, 148
Gessner, 295
Geyer, 410

Giant salamanders, 48, 468
Giersberg, 323, 341
Giesbrecht, 327
Gigantism, 298
Gigantorana, 519
Gigantorana goliath, 519
Gill, arches, 223

bell-shaped, 54, 60

clefts, 186

external, 101, 160, 162

form, 161

internal, 160, 162

regeneration of, 36

relation of form to function, 161

slits, 185

Gills, 3, 5, 25, 28, 31, 34, 48, 51,
57, 58, 68, 72, 102, 103, 158-
160, 164, 176, 182, 187
Girdles, 184

arciferal type of, 236

firmisternal, 101

firmisternal type of, 236

pectoral, 101, 234, 244

pelvic, 237
Giusti, 304

Giusti and Houssay, 299

Giusti, Houssay, and Gonzalez, 299

Glands, 3, 95

alveolar, 132

carotid, 191

chin, 136

cloacal, 284

endocrine, 102, 290-316

556

THE BIOLOGY OF THE AMPHIBIA

Glands, granular, 132-134, 137

hatching, 23, 131

hedonic, 388, 389

intermaxillary, 202

of internal secretion, 35

modification of, 95

mucous, 132-134, 136, 137

naso-labial, 137

parotoid, 132, 514

pelvic, 285

pituitary, 296

poison, 133

thyroid, 291

tubular, 132, 136
Glandular fold, 201
Glandular hypertrophies, 119, 120

in male, 114, 136
Glandular outgrowths, 205
Glenoid cavities, 38
Glenoid region, 236
Gley, 304

Gley and Brossard, 305

Glomerular capsule, 268, 270

Glomerulus, 268

Glomus, 267

Glossopharyngeus, 263

Glottis, 168, 171, 172, 174, 184

Glucose, 206, 208

Glutaeus, 262

Glycogen, 206-208

Glyphoglossus, 532, 533, 535, 537,

538
Goetsch, 437
Goldfederowa, 302
Goldschmidt, 86
Goldsmith, 403, 406, 415, 421
Goldsmith and Beams, 204
Golgi bodies, 18
Goliath frog, 13
Goltz, 366

Gonads. 108, 110, 208, 305

segmentation of, 280
Goodrich, 222
Gopher frog, 97
Goppert, 205
Goss, 184

Gottschalk and Nonnenbruch, 266
Gracilis, 262
major, 260

Gracilis, minor, 260
Gradients, 36

Granulocytes, 179, 182-184
Gray, 268, 270

Gray crescent, 19, 21, 22, 26, 35, 36

Greene and Laurens, 339

Gregory, 3, 241

Gregory and Noble, 219

Greil, 160, 166

Grinnell, 82

Grodzinski, 185, 195

Groebbels and Kuhn, 310

Growth, rate of, 436

Gruenberg, 339

Grypiscus, 499

Guanophores, 141, 143, 144, 146,

148, 151
Gudernatsch, 293
Guyenot and Ponse, 40, 440
Gymnophiona, 12, 76, 159, 165, 230-

232, 244; 283, 321, 328, 329,

333, 357-^60, 367, 463-465
Gyrinophilus, 55, 57, 124, 285, 333,

417, 418, 423, 479, 480
Gyrinophilus danielsi, 100, 413
Gyrinophilus porphyriticus, 100, 124,

433

Habenula, 362
Haber, 415

Habitat preference, 97
Habits, 377

breeding, 402

feeding, 415

motor, 394
Hadjioloff, 208
Haecker, 82, 147, 148, 394
Haemal arches, 232
Haemoglobin, 158, 179, 180
Hairy Frog, 110, 164, 517
Hall, 273

Hall and Root, 433
Hankinson and Adams, 457
Hargitt, 145, 417
Harington, 296

Harms, 4, 39, 110, 138, 278, 307
Harrison, 26, 28, 29, 33, 35, 440

INDEX

557

Hartmann, 436
Hatching of Alytes, 131
Hay, 435
Hayman, 268
Head, 97

Head structure of Gastrophryne

carolinensis larva, 24
Hearing, 341

Heart, 34, 111, 185-187, 189, 190,
208, 248
function of, 193
modifications of, 192
muscles, 247
output, 193

of Rana catesbeiana, 190
rate, 193

of Siren lacertina, 193
Hecht, 420

Hedonic glands, 109, 118, 137, 388,

389
Heesen, 180
Hegner, 439
Heidenhain, 283
Heleophryne, 498
Heleophryninae, 498
Helff, 31, 103, 292, 434
Heliarchon, 476
Helioporus, 97, 497
Hemidactylium, 58, 59, 91, 126, 127,

285, 389, 402, 414, 426, 481, 482
cleavage in, 21
limb development in, 33
Hemidactylium scutatum, 481
Hemidactylium scutatum larva, C9
Hemimantis, 525, 526
Hemiphractinae, 508-510
Hemiphractus, 60, 125, 499, 509,

511, 526
Hemisinae, 527, 540
Hemisus, 64, 538, 540
Hemisus marmoratum, 111
Hemosporidia, 440
Hempelmann, 396
Henderson, 457
Henle's loop, 269, 270
Hepatic duct, 205
Hepatic portal vein, 186
Herbst, 149
Hereditary factors, 19

Hereditary mechanism, 86, 87

Hereditary units, 81

Heredity and development, 15-47

Hering, 371

Herlant, 19

Heron-Roy er, 41

Herrick, 5, 323, 356, 358-360, 362,

364, 369
Herter, 337, 339
Hertwig, 21, 38, 41, 42
Herwerden, 304
Hess, 344

Heteroclitotriton, 476
Hibbard, 16, 17
Hibernation of frogs, 418
Hildebrandtia, 520
Hill, 151, 434
Hilton, 184
Hilzheimer, 127
Hind limbs, 186

in frog and salamander larvae, 25

musculature, 259
Hindbrain, 357

Hinsche, 381, 384, 395, 410-412,

423, 424
Hodge, 415
Hoffman, 465
Hogben, 301, 304
Hogben and Winton, 300
Holl, 438, 441

Holldobler and Schulze, 310
Holmes, 412, 418
Homing, 404, 405

instinct, 403

visual impressions, 404
Homology, basis of, 31, 32

of muscle, 248
Hopkins, 323, 324
Hoplophryne, 68, 162, 539
Hoplophryne rogersi, 118
Hoplophryne tduguruensis, 117, 118
Hoplophryninae, 539, 540
Hormones, 39, 102, 146, 151, 179,
194, 296, 300

in evolution, 98

and metabolism, 434

testicular, 109
Horny claws, 49
Horny growths, 138

558

THE BIOLOGY OF THE AMPHIBIA

Horny plates, 67

Hoskins, E. R., and M. M., 293

Houssay and Giusti, 299

Houssay, Giusti, and Gonzalez, 299

Houssay and Ungar, 145

Howes and Ridewood, 243

Howes and Spaul, 299

Howland, 271

Hubbard, 423

Humerus, 118, 240, 241

Humidity, 433

change, responses to, 421
Humphrey, 21, 22, 277, 279, 280, 307
Hunger contractions, 347
Hunting instinct, 390
Huxley, 292

Huxley and Belehradek, 296, 300
Huxley and Fulton, 301
Hybridization, 40-42

and origin of species, 42
Hybrids, 40, 87

false, 40

Hydromantes, 59, 125, 276, 449,

454, 482, 483
Hydromantes genei, 137, 422, 483
Hydromantes italicus, 133, 137, 310,

328, 483

Hydromantes platycephalus, 125, 483
Hydrostatic organs, 62, 87, 167, 168,
240

Hyla, 66, 68, 69, 88, 99, 120, 151,
153, 407, 408, 423, 451, 456,
508-514, 526

Hyla andersoni, 87, 97, 152

Hyla arbor ea, 111, 180, 347

Hyla arborea japonica, 276

Hyla arborea meridionalis, 508

Hyla arenicolor, 97, 152, 409, 436,
444, 454

Hyla brunnea, 88

Hyla caerulea, 409

Hyla cinerea, 415

Hyla crucifer, 72, 95, 406, 407, 419

Hyla dominicensis, 88, 97, 512

Hyla faber, 68

Hyla goughi, 146

Hyla heilprini, 118

Hyla humeralis, 118

Hyla leprieuri, 111

Hyla lichenata, 512, 513

Hyla maxima, 118, 509

Hyla nasuta, 510

Hyla nigromaculatus, 512

Hyla phaeocrypta, 408

Hyla pollicaris, 118

Hyla pulchella, 513

Hyla regilla, 97, 408

Hyla rosenbergi, 68, 404

Hyla (Nyctimantis) rugiceps, 511

Hyla uranochroa, 69, 119, 513

Hyla vasta, 95, 96, 99, 134, 512, 513

Hyla venulosa, 426

Hyla versicolor, 62, 69, 144, 152,

344, 408, 419, 436
Hylaeobatrachus, 465
Hylambates, 67, 112, 524-526
Hylarana, 521, 522
Hylella, 508

Hylidae, 67, 70, 90, 118, 130, 329,

408, 448, 495, 508-514, 524, 526
Hylinae, 509, 510-514
Hylodes petropolitanus, 75
Hylonomidae, 463
Hylonomus, 243
Hylophorbus, 533
Hylorina, 499
Hylorina sylvatica, 500
Hyloxalus, 507
Hymenochirus, 231, 489-491
Hynobiidae, 48, 49, 51, 138, 146,

226, 282, 283, 386, 448, 466-

468, 472
fertilization in, 16
Hynobius, 51, 80, 92, 150, 159, 274,

275, 343, 357, 466, 467
eggs, larvae, 49

number and size, 48
Hynobius keyserlingii, 468
Hynobius kimurai, 468
Hynobius lichenatus, 273, 386
Hynobius peropus, 467
Hynobius vandenburghi, 466
Hyobranchial apparatus, 30, 101,

102, 159, 224, 226
Hyobranchial muscles, 254
Hyoid, 159, 162, 166, 170, 173, 223,

226

Hyomandibular, 6, 221

INDEX

559

Hypaxial musculature, 249, 251

Hyperolia, 76, 498

Hyperolius, 67, 408, 452, 524, 525

Hypnotic response, 381

Hypnotic state, 424

Hypobranchial, 249

Hypogeophis, 76, 166, 216, 230,

367, 463
Hypoglossal fenestra, 213
Hypoglossal nerves, 213, 366
Hypopachus, 532, 536, 537
Hypophysectomy, 40, 140
Hypophysis, 23, 28, 297
Hypothalamus, 362

Ichthyophis, 76, 463, 465
Ichthyophis glutinosus, chondrocran-

ium of, 219
Identification of sex, 285
Ileolumbaris, 250
Ilia, 240

Iliacus externus, 262
Ilioextensorius, 262
Hiofibularis, 262
Diotibialis, 262
Ilium, 7, 239, 262
Immobility, tonic, 424
Impulses, sympathetic, 248
Individuation of reflexes, 34
Indobatrachus, 498
Inferior colliculus, 363
Inferior labial cartilage, 24, 30
Infundibulum, 296, 298
Inguinal blotches, 153
Inguinal glands, 120
Inner ear, 222, 338
Instinct, brooding, 413, 414

homing, 403

hunting, 390

and intelligence, 377-398

mechanism of, 390

parental, 412

patterns, 396

phylogenetic change of, 384
Insulin, 301

Integument, 3, 31, 35, 96, 130-
157, 182

Integument, in respiration, 163

vascularity of, 182
Intelligence, 395
Intercentrum, 8, 228
Interclavicle, 7, 234
Interdorsals, 227
Intergeneric crosses, 41
Intergrades, 91
Intermedium, 33, 242
Internal fertilization, 88
Internal nares, 171, 173, 213
Internal respiration, 158
Interpterygoid vacuities, 8, 213
Interrenal tissue, 303

function of, 304
Intersegmental vein, 195
Interstitial cells, 305
Intertemporals, 213
Interventrals, 227
Intestinal diverticula, 165
Intestinal epithelium, 183, 207
Intestinal glands, 206
Intestines, 111, 203, 205-207, 209

effect of food on, 209

in frog larvae, 55

in frog tadpoles, 25

large, 208
Intromittent organ everted, 464
Inukai, 194

Iodine and metamorphosis, 295
Iriki, 276
Iris, 326, 329
Ischiadic vein, 196
Ischioflexorius, 260, 262
Ischium, 239

Islets of Langerhans, 205, 301
Isolation, 82
kinds of, 83

in species formation, 82
Isserlin, 432
Isyama, 197

Jacobshagen, 160, 204
Jacobson's organ, 325, 358
Jaws, 62, 102, 166, 222, 244

changes in, 219

compared, 220

560

THE BIOLOGY OF THE AMPHIBIA

Jaws, lower, 213

muscles, 263

tubercle on lower, 172
Jensen, 294
Johnson, 150

Johnston and Cleland, 440
Jolly and Lieure, 197
Jordan, 85, 412

Jordan and Speidel, 180, 182, 183
Jugal, 212

Jugulars, external, 186
internal, 186

Kahn, 110

Kalophryninae, 45, 451, 506, 536,
537

Kalophrynus, 62, 536, 537
Kaloula, 62, 536, 538
Kaloulinae, 538
Kammerer, 93, 194
Kampmeier, 195
Kandler, 110, 111
Kappers, 365
Kassina, 67, 524, 525
Kassina senegalensis, 67, 526
Keith, 173
Kellicott, 80
Kellogg, 415
Kennel, 281
Kenyon, 431

Kidney, 183, 186, 193, 208, 266,
269

function of, 270

metanephric, 269

regulatory mechanism of the
amphibian, 272
Kiesewalter, 358, 359
Kingsbury, 184, 202, 206, 319
Kingsbury and Reed, 222
Kingsley, 244
Kirkland, 415
Kleine, 309
Klier, 110
Klinge, 387

Klingelhoffer, 109, 114, 282, 388,

417, 454
Kohl, 333
Komine, 110

Koppanyi and Pearcy, 411
Korschelt, 36, 37
Kraupl, 193
KrefTt, 409

Krizenecky and Petrov, 210

Krogh, 174, 301, 431

Krohn, 437

Kropp, 145, 146

Kriiger and Kern, 151

Kuhlenbeck, 359, 362, 365, 367, 369

Kuhn and Groebbels, 310

Kuki, 270

Kunde, 422

Kunitomo, 400

Kuntz, 373

Kurepina, 323

Kuroda, 343

Kyle, 115

Labyrinth, membranous, 334, 335,
336

Labyrinthodontia, 6, 8-10, 76, 130,
201, 214, 216, 221, 226, 227,
234, 257, 459-461

Lacrimal bone, 215, 328

Lacrimal duct, 329

Lacrimal gland, 3

Lactic acid, 158

Lagena, 336

Land bridges, 451

Langendorff, 412

Langerhans, islets of, 205, 301

Langlois and Pellegrin, 422

Lankes, 409

Lankesterella, 441

Lantz, 94

Lapicque and Petetin, 175
Large intestine, 205
Larger parasites, 441
Larson, 299

Larvae 1, 23-25, 50, 171
Larvae, permanent, 102, 470
Larval life, 13
Larval teeth, 76, 139

tail and gills, 25
Larjmgeal cartilages, 169, 226
Laryngeal skeleton, 226
Larynx, 168-170, 174

INDEX

561

Lateral-line canals, 212
Lateral-line nerves, 319
Lateral-line organs, distribution of,
320

relation of color pattern to, 148
Lateral-line sense organs, 53, 79,

148, 318, 319
Latissimus dorsi, 257
Latreille, 2
Laubmann, 326
Laurens, 145, 431
Laurens and Greene, 339
Leaping of salamanders and frogs,

425

Learned behavior, 392
Lebrun, 282
Lechriodus, 497, 498
Lechriodus melanopyga, 113
Legs, 12

regeneration of, 36
Lehmann, 32
Length of life, 443
Lens, 28, 29, 37, 326

regeneration of, 37
Lepidosiren, 164

Lepospondyli, 4, 10, 11, 231, 234, 462
Leptobrachella, 493
Leptobrachium, 492
Leptobrachium carinense, 382
Leptodactylidae, 72, 496
Leptodactylinae, 504-505
Leptodactylodon, 518
Leptodactylus, 68, 72, 120, 504, 505
Leptodactylus ocellatus, 68, 110, 117,
145

Leptodactylus pentadactylus, 135, 404
Leptopelis, 67, 153, 524-526
Leptopelis aubryi, 119
Leptopelis brevirostris, 125, 518
Leptopelis rufus, 119
Leptopelis tessmanni, 42
Leptorophus tener, 10
Leucocytes, 179, 184
Leurognathus, 202, 480, 481
Leurognathus marmorata intermedia,
122

Leurognathus marmorata marmorata,

122
Levy, 420

Lewis, 256

Ley dig, 115

Leydig cells, 102

Liang, 270

Lichtenstein, 438

Life, length of, 443

Life history, mode of, 48-78, 75

Light stimulations, 146

Limbs, 4, 7, 33, 103, 240, 244

development of, 32, 33

hind, 256

modification of, 138

muscles, 247, 249

secondary, 38-39
Limnerpetontidae, 463
Limnodynastes, 76, 497
Limnodynastes dorsalis, 114
Limnodynastes tasmaniensis, 282
Limnomedusa, 504
Lindeman, 34, 149, 328
Linden, 147
Linnaeus, 2

Liopelma, 234, 257, 485

ventral body muscles, 255
Liopelmidae, 75, 76, 229, 231, 234,

448, 462, 485-486, 495
Liophryne, 531
Liophryne rhododactyla, 531
Lipase, 207

Lipophores, 141, 143, 144, 148, 150,
151

Litzelmann, 335

Liver, 110, 180, 205, 207, 208

Locher, 340

Locomotion, 6, 92

modes of, 247
Loeser, 360, 364, 370
Lohner, 380
Lophyohyla, 511
Lower jaw, 213
Lower limb bones, 243
Loxommidae, 460
Lubosch, 263

Luckhardt and Carlson, 176
Lullies, 411
Lunglessness, 173

Lungs, 5, 62, 87, 110, 141, 158, 162,
164-166, 168, 170-173, 186, 187,
189, 190, 192

562

THE BIOLOGY OF THE AMPHIBIA

Lungs, comparison of, 167

in frog and salamander larvae, 25

rudiments, 165
Luther, 29
Lutz, 75, 419
Lydekkerinidae, 460
Lymph, 115, 195
Lymph hearts, 195, 197
Lymphatic vessels, 195, 196
Lymphocytes, 179, 182-184
Lymphoidal tissue, 184
Lysorophus, 11, 160, 463

Macela and Seliskar, 159
Macropelobates, 494
Macrophages, 182, 183, 197
Manculus, 55, 91, 124, 479, 481

limb development in, 33
Mandible, 220

larval, 52
Mangold, 27, 34, 37, 249, 424
Mangold and Eckstein, 425
Mantella, 525, 526
Mantidactylus, 525, 526
Mantipus, 530
Mantophryne, 64, 535, 536
Mantophryne macrops, 536
Marbled salamander, 472
Marcus, 159, 165, 166, 169, 170,

174, 195
Marcus and Blume, 230, 232
Marine Toad, 135
Marsupial frogs, 54, 59, 160, 509
Martin, 363

Martin and Armistead, 304
Marx, 300
Masseters, 264
Mastodonsauridae, 461
Mating instinct, 390
Matthes, 324, 340, 417
Matthew, 85, 452
Matthews and Detwiler, 380
Maurer, 103, 141, 208, 252, 253,
308

Mauthner's cell, 369
Maxillary, 102, 103, 215, 218
Maximow, 183

Mayenne, 443
McAtee, 405, 418
McClure, 438
McCord and Allen, 310
McDonald, Leisure, and Lenneman,
202

McKibben, 360
McNally and Tait, 338
Meantes, 465, 484
Mechanoreceptors, 339
Meckel's cartilage, 25, 220
Medialia, 33, 242
Median eye, 309
Medulla, 176, 194, 365
motor portion of, 366
Medulla oblongata, 357
Megaelosia, 504, 534
Megalixalus, 112, 452, 524, 525
Megalixalus fornasinii, 113
Megalixalus leptosomus, 113
Megalixalus spinosus, 113
Megalobatrachus, 13, 48, 103, 162,

184, 226, 257, 267, 274, 326,

399, 410, 443
Megalobatrachus japonicus, 468, 469
Megalobatrachus maximus, 443
Megalophrys, 69, 101, 119, 423, 492,

493

Megalotriton, 476
Megophryinae, 492
Mekeel, 168
Melanin, 144, 148, 149
Melanism, 150
Melanobatrachinae, 538-539
Melanobatrachus, 538, 539
Melanophores, 141, 143, 151
Memory, associative, 392

muscle, 395, 404
Mental bone, 221

Mento-Meckelian bones, 24, 172, 264
Mertens, 80, 120, 422
Mesenchyme, 30, 147, 195
Mesenteries, 205
Mesoderm, 30, 184
Mesomere, 267

Mesonephric tubules, 268, 275
Metabolic rate, 180, 210, 431
of breeding season, 434

INDEX

563

Metabolism, 110, 179, 185, 206, 431

and behavior, 434

calcium, 308

and environment, 432

hormones and, 434

starvation, 434
Metacarpus, 117

Metamorphosis, 25, 30, 50, 103,
292, 293, 295

iodine and, 295, 296

part of mechanism of, 30

thyroid and, 292
Metanephric kidney, 269
Metatarsal tubercles, 96
Metcalf, 88, 440
Metoposauridae, 461
Mibayashi, 267
Michaelsen, 441
Micrixalus, 521-523
Microbrachidae, 463
Microhyla, 101, 510, 537, 538
Microhyla achatina, 69
Microhyla heymonsii, 69
Microhyla rubra, 537
Microhylinae, 451, 506, 537-538
Micropholidae, 460
Microsaurs, 130
Microscopic parasites, 438
Midbrain, 357, 362, 367, 369
Migration, 399, 400, 401, 403

humidity and temperature, 422

routes, probable, 450
Mimicry, 90
Miner, 241, 258, 259
Mitrolysis, 497
Mixed nerves, 370
Mixophyes, 497
Mode of life history, 48-78
Modern amphibia, 12
Moesel, 53
Molt, 139
Monakow, 360
Monilia, 438

Monocytes, 179, 182, 183
Montsechobatrachus, 485
Moore, 185

Morgan, 80, 82, 83, 108, 127, 322,
419

Mosaic formation, 26

Moszkowski, 21

Mountain-brook inheritance, 49
Mountain-brook larvae, 51
Mountain-brook newts, 114
Mouth, 66, 70, 74

parts, modification of, 69

tadpole, 63
Movements, coordination of, 371

swimming, 379
Muchin, 366
Mucin, 134

Mucous cells, 202, 203
Mud Puppy, 484
Muhse, 139
Muller, 209
Muller, 85

Muller-Erzbach, 420
Mullerian duct, 272, 276, 281
Munz, 415

Muscle memory, 395, 404
Muscles, body, 249

extensor and flexor, 259

forelimb, 255

heart, 247

homology, 248, 259

hyobranchial, 254, 263

jaw, 263

non-striated, 247

pectoralis, 258

smooth, 301

striated, 247

subhyoid, 170

temporal, 215

visceral, 263
M. intern eurales, 250
M. intertransversarii, 250
M. longissimus dorsi, 250
M. obliquus externus, 252
M. obliquus internus, 252
M. rectus abdominis, 252
M. rectus lateralis, 252
M. rectus profundus, 252
M. rectus superficial, 252
M. transversus, 252
Muscular system, 247-265
Musculature, arm and shoulder, 256

common type of, 260

dorsal, 250

of head, 263

564

THE BIOLOGY OF THE AMPHIBIA

Musculature, hind limb, 259

tail, 249

tongue, 226

ventral, 234, 251, 254
Mushroom tongue, 201
Mutations, 80, 81, 86
Myers, 184
Myobatrachus, 498
Myocommata, 248, 250, 251
Myoseptum, 227, 249
Myotomes, 247

Naef, 233

Nakamura, 109, 307
Nannobatrachus, 518-519
Nannophrys, 519
Nares, 172
Nasal bone, 215
Nasal capsule, 29, 172, 216
Nasal chamber, mechanism of clos-
ing, 172
Nasal passage, 3
Naso-labial glands, 137
Naso-labial grooves, 124, 136
Natalobatrachus, 66
Natural selection, 85, 86, 93
Nectodactylus, 536, 537
Nectophryne, 503

Nectophrynoides, 74, 273, 494, 501,

502, 503
Nectophrynoides tornieri, 409
internal fertilization in, 15
Nectophrynoides vivipara, 74, 501
Nectridia, 11, 463

Necturus, 40, 50, 98, 102-104, 145,
147, 162, 164, 167, 176, 180,
187, 206, 215, 226, 233, 234,
256, 275, 284, 285, 293, 298,
308, 326, 331-335, 341, 344,
347, 358, 360, 363, 364, 367,
391, 392, 414, 416, 421, 443,
449, 453, 483, 484

Necturus maculosus, development of,
20

vascular system of, 188
viscera of, 203

N. maculosus lewisi, 98, 99, 484
N. punctatus, 484
Nematodes, 441
Neoteny, 104
Nephrostomes, 267
Nerve endings, free, 321
Nerves, 38

hypoglossus, 366

mixed, 370

spinal, 369

spinal cord and, 369
Nervous mechanisms, 146
Nervous system, 33, 353-376
Nervus terminalis, 360
Nesobia, 493
Nesomantis, 495
Nesomantis thomasseti, 494
Neural arch, 230
Neural crest, 370
Neural plate, 26, 32, 357, 369
Neural tube, 27
Neuro-motor mechanism, 378
Neurons, 353
Neutrophiles, 183
Newts, 166, 167, 171

archenteron in, 31

European, gastrulation in, 21
hybridization in, 40

regeneration of hyoid in, 36

regeneration of limbs in, 36

regenerative capacity in, 39

transplanting neural plate, 32
Nicholas, 34, 340, 371, 417
Nictitating membrane, 328
Nieden, 465
Niemack, 322
Nikitin, 164

Noble, 2, 42, 52, 62, 64, 68, 73, 102,
111, 123, 124, 131, 139, 148,
168, 173, 189, 226, 241, 258,
260, 293, 295, 415, 416, 418,
440, 451, 507, 508, 517, 543,
579

Noble and Brady, 131, 138, 389, 390
Noble and Farris, 103, 112, 113, 115,
410

Noble and Jaeckle, 95

Noble and Noble, 97, 400, 404

INDEX

565

Noble and Parker, 529

Noble and Pope, 16, 93, 98, 284, 305

Noble and Richards, 299

Noble and Weber, 284

Norris, 333, 337

Nose, 28

Nostrils, 99, 170

Notaden, 498

Notochord, 31, 227, 230, 232
Notophthalmus, 475
Nototrema, 509
Nucleus, 180, 181

Nuptial pads, 108, 109, 111, 112,
117

Nussbaum, 282
Nyctibates, 517
Nyctibatrachus, 518
Nyctimystes, 508, 513

Oak toad, 73
Obreshkove, 332
Obturator foramen, 239
Occipital, 214
Occiput, 244, 249
Oculomotor, 361
Odors, 137
Oedipina, 482

Oedipus, 59, 95, 99, 146, 454, 482,
483

Oesophagus, 202
Okada, 83, 456
Okajima, 326, 329
Okajima and Tsusaki, 327
Olfactory centers, 3
Olfactory epithelium, 323, 324
Olfactory hairs, 324
Olfactory lobes, 357
Olfactory nerves, 357
Olfactory organs, 321, 323
Olfactory sense, 412
Olfactotactile center, 360
Olfactovisceral center, 360
Oliver and Eshref, 271
Olm, 483
Olmsted, 302
Omohyoideus, 255
Omostcrnum, 237

Omphalo-mesenterics, 185
Ontogeny, 101

Onychodactylus, 49, 52, 138, 274,

275, 467
Onychodactylus fischeri, 467
Onychodactylus japonicus, 467

larvae of, 138
Ooeidozyga, 489, 519
Ooeidozyga laevis, 519
Ooeidozyga semipalmata, 519
Opalina ranarum, 439
Opalinid parasites, 88, 439
Opercular sac, 24, 25
Operculum, 103, 160, 162, 171, 221
Ophryophryne, 493
Opisthocoela, 486
Opisthocoelus vertebra, 9, 229
Opisthotic, 215
Optic centers, 3
Optic cup, 28, 37
Optic radiation, 362
Optic vesicles, 360
Oreobatrachus, 519
Oreophryne, 532, 536
Oreophrynella, 231, 505-507
Organizers, 26, 27, 38
Organs, adrenal, 302

of chemical sense, 321

lateral-line, 318

olfactory, 323

pineal, 309

tactile, 321

of taste, 322

urogenital, 266
Os thyreoideum, 225
Osmotic conditions, 77, 193
Ossification in skin of Salientia, 512
Osteolepidae, 5, 7, 213
Osteolepis, 213
Otic capsule, 6, 37, 221, 335
Otic notch, 213
Otophryne, 536
Ovarian sacs, 277
Oviducts, 59, 94, 282

gravid Salamandra, 54
Ovocyte, developing, 281
Ovogonia, 277
Ovo viviparity, 15, 59, 74

566

THE BIOLOGY OF THE AMPHIBIA

Ovulation, 281

Oxydactyla, 531

Oxygen, 68, 158, 179, 182, 207

consumption, 431
Oxyglossus, 498, 519
Oxyglossus laevis, 519
Oxyglossus semipalmata, 519
Oxyhaemoglobin, 159

Pachypalaminus, 466, 467
Pachytriton, 218, 474, 475
Pack, 416
Pads, friction, 521

nuptial, 108, 111, 117
Pain cry, 409

Palaeobatrachidae, 449, 495-496
Palaeobatrachus, 495
Palaeobatrachus diluvianus, 496
Palaeobatrachus luedecki, 495, 496
Palate, 102, 215, 216, 217, 218
Palato quadrate, 25, 102, 218
Pallial cortex, 360
Palmatorappia, 524
Palmer, 332

Paludicola, 71, 72, 496, 504, 505
Pancreas, 205, 206, 301
Pancreatic juice, 206
Papilla basilaris, 336, 337
Parachordal cartilages, 230
Parallelism, 91, 153
Parapophyses, 232
Parasites, 438, 441
Parasphenoid, 214, 216
Parasympathetic, 371
Parasympathetic impulses, 248
Parathyroids and ultimobranchial

body, 307
Parental instinct, 412
Parhoplophryne, 539
Parietal bones, 215
Parker, 321, 330, 343, 504
Parmenter, 41
Parotic crest, 222
Parotoid glands, 120, 514
Pars anterior, 298, 299
Pars intermedia, 145, 146, 297, 298,

300

Pars nervosa, 298

Pars posterior, 298, 300

Patch, 150, 295

Patterson, 348

Pawlas, 149

Pearse, 344, 421

Pectineus, 260

Pectoral amplexus, 76

Pectoral girdles, 6, 7, 9, 90, 234, 235,

237, 244, 528
Pectoral muscles, 257, 258
Peduncles, 73
Pelion, 9
Peliontidae, 462
Pellegrin and Langlois, 422
Pelobates, 97, 119, 151, 296, 335,

343, 493, 494
Pelobates fuscus, hybridization in, 41
Pelobatidae, 75, 76, 111, 119, 130,

226, 230, 243, 258, 448, 491,

492-495, 496, 498
Pelobatinae, 492, 493-494
Pelodytes, 111, 137, 243, 493, 494
somatic number of chromosomes
in, 18

Pelodytes punctatus, 113 '

Pelophilus, 489

Pelvic embrace, 75, 76

Pelvic girdle, 237, 256

Pelvic gland, 16, 285

Pelvis, 7, 187, 231, 237, 238, 244,

249, 259
Pentimalli, 183
Pepsin, 206, 207, 208
Peredelsky and Blacher, 151
Perennibranchs, 98, 104, 166, 170,

180, 254
Pericardial cavity, 163, 195
Perichordal sheath, 227
Perilymphatic duct, 337
Peritoneal cavity, 151, 195
Peritoneum, 203, 205
Permian urodele, 463
Pernitzsch, 148
Peter, 222
Petrohyoidei, 263
Petromyzon, 291, 310
Petropedetes, 121, 521
Petropedetes newtoni, 117, 120

INDEX

567

Petropedetes palmipes, 521
Petropedetinae, 520, 521
Phagocytosis, 182
Phalangeal formula, 243
Phalanges, 95, 243, 508
Phanerotis, 497
Pharyngeal movements, 176
Pharynx, 165, 168, 187
Philautus, 525
Philocryphus, 497
Philoria, 498
Phisalix, 133, 134, 137
Pholidogasteridae, 460
Photosensitive cells, 330
Phototropic response, 401
Phototropism, 344, 419
Phractops, 497
Phrynella, 537

Phrynobatrachus, 66, 112, 515, 516
Phrynoderma, 525
Phrynomantis, 533, 534
Phrynomerinae, 538
Phrynomerus, 538
Phrynomerus bifasciata, 134
Phrynopsinae, 518
Phrynopsis, 518
Phrynopsis boulengeri, 518
Phrynopsis ventrimaculata, 518
Phrynopsis usumbarae, 125
Phyllobates, 60, 69, 70, 95, 152,

415, 507
Phyllobates nubicola, 113
Phyllomedusa, 69, 95, 282, 401,

513, 514
Phyllomedusa bicolor, 613
Phyllomedusa calcarifer, 513
Phyllomedusa moreleti, 513
Phyllomedusa perlata, 514
Phyllomedusa spurrelli, 513
Phyllospondyli, 4, 9, 10, 11, 234,

461-462, 465
Phylogeny, 101

of brain, 367

course of, 104

function in, 91

of Salientia, 486

of secondary sex characters, 116
of urodeles, 469
Physalaemus, 504, 505

Physiological characters, 97-98
Piersol, 84, 329, 400
Pigmentation, 141

influence of the environment on,
149

Pigmentless eggs, 55
Pike, 339

Pineal foramen, 8, 214, 309

Pineal organ, 309, 361

Pipa, 60, 76, 96, 168, 226, 309, 335,

362, 363, 414, 418, 491
Pipa pipa, 491

Pipidae, 75, 111, 138, 162, 168,
197, 202, 221, 222, 226, 230,
233, 318, 319, 418, 448, 486,
489-491, 495

Pipinae, 491

Piquet, 277

Pituitary gland, 35, 145, 151, 195,

296, 297, 300, 301
Pituitrin, 195
Placoid scales, 219
Plagiosternum, 461
Plasma, 179, 197
Plasma proteins, 193
Plasmocytes, 179
Platyhyla, 530, 536
Platymantis, 522, 523
Platymantis solomonis, 522, 523
Platypelis, 530
Plectromantis, 504
Plethodon, 57-59, 86, 91, 97, 126,

127, 132, 286, 298, 402, 414,

424, 426, 454, 481-483
Plethodon cinereus, 57, 58, 84, 86,

126, 152, 182, 283, 422, 424,

443, 444

Plethodon glutinosus, 84, 97, 132,

153, 421, 423, 433
Plethodon jordani, 90
Plethodontid salamanders, gastrula-

tion in, 22
Plethodontidae, 55-57, 58, 74, 91,

126, 136, 146, 148, 167, 215,

216, 285, 298, 389, 448, 453,

475, 477-483, 529
Plethodontohyla, 530
Pleurocentrum, 8, 9, 228, 229

568

THE BIOLOGY OF THE AMPHIBIA

Pleurodeles, 52, 109, 387, 475
fixation of limb axes in, 33
Pleurodeles poireti, 109
Pleurodeles waltl, 109, 233, 401, 443,
475

Pleurodelidae, 474
Pleurodema, 72, 504
Plicognathus, 469
Pogonowska, 150
Poison glands, 133
Poisonous secretions, 134
Polar bodies, 281
Polarization, 33
Policard and Bonnamour, 304
Poll, 40

Polypedates, 66, 67, 69, 72, 153,
452, 521-524, 526

Polypedates arborea, 83

Polypedates dennysi, 457, 624

Polypedates malabaricus, 426

Polypedates nigropalmatus, 426

Polypedates schlegelii, 83

Polypedatidae, 66, 90, 237, 520,
624-526

Polysemia, 476

Polyspermy, 282

Polystomum, 441

Ponder, 180

Ponse, 278, 305

Ponse and Guyenot, 440

Pope, 112, 457

Popow and Wagner, 176

Postcardinals, 185, 186, 195, 267

Posterior limbs, regenerative capac-
ity in, 39

Postfrontal, 213

Postma and Dolk, 434

Postminimus, 242

Postorbital, 212

Post-temporal, 234

Power, 42, 67

Preadaptation, 94

Prearticular, 213, 220

Prefrontals, 215

Prehallux, 242, 244

Prehensile organs, 253

Premaxillaries, 24, 172, 201, 215, 221

Premaxillary teeth, 109

Prenasal superior process, 172

Prepollex, 108, 111, 112, 117, 118,

126, 241, 242
Prepubis, 240
Presacral vertebra, 231
Preservation reflexes, 391
Prevomers, 216
Procoela, 495, 496, 505, 514
Procoelous vertebra, 9, 229
Procoracohumeralis, 258
Procoracoid, 236, 258
Pronephros, 33, 185, 267
Prootic, 215

Propagation, ways of, 74
Proprioceptive centers, 363
Prostate, 287
Protective coloration, 152
Proteida, 465, 483

Proteidae, 50-51, 448, 449, 483-484
Proteins, 205, 208

Proteus, 50, 92, 97, 103, 104, 132,
134, 146, 149, 166, 180, 203,
208, 210, 244, 275, 276, 293,
295, 326, 331, 333, 358, 449,
483

Proteus anguinus, 115
Protopelobates, 489, 495
Protopipa, 60, 76, 96, 414, 489, 491,
495

Protozoa, 438, 440
Protractor lentis, 329
Przibram, 37
Przylecki, 271
Pseudacris, 407, 510, 511
Pseudacris nigrita, 407
Pseudacris ocularis, 407
Pseudacris triseriata, 407
Pseudhymenochirus, 489, 491
Pseudinae, 496, 497, 499-500, 504
Pseudis, 320, 497, 499
Pseudis paradoxa, 98, 444
Pseudobranchus, 50, 97, 103, 161,

162, 236, 436, 484, 485
Pseudobufo subasper, 503
Pseudohemisus, 529
Pseudophryne, 76, 498, 501
Pseudophryne guentheri, 120
Pseudoteeth, 125
Pseudotriton, 100, 152, 497
Pseudotriton montanus, 55

INDEX

569

Pseudotriton ruber, 55, 173, 202, 479
Pternohyla, 508, 509, 512
Pterygoideus, 264
Pterygoids, 216, 218
Pubis, 239, 240

Puboischiofemoralis internus, 260,
262

Puboischiotibialis, 260
Pubotibialis, 260
Puente, 300
Pulmonary arches, 190
Pulmonary circulation, 172
Pulmonary respiration, 171
Pulmonary vein, 186, 189
Pulsation, rate of, 193, 194
Pupil, 92, 118, 329

form, 90
Pycraft, 113
Pylangium, 189, 190
Pyloric caeca, 208
Pylorus, 203, 205
Pyriform, 358
Pyriformis, 262

Quadratojugal, 215, 264
R

Rachitomi, 2, 8, 221, 223, 227, 229,

236, 242, 406, 460
Radiale, 242
Radius, 240, 241
Ramanella, 538

Ramus communicans, 370, 371
Rana, 41, 48, 62, 64-66, 76, 80, 91,
97, 111, 120, 132, 141, 145,
191, 197, 202, 203, 222, 230,

237, 258, 276, 282, 294, 300,
310, 323, 328, 331, 332, 342,
343, 381, 393, 395, 423, 442,
444, 449, 456, 498, 506, 510,
514-516, 518-522, 526, 528,
540

archenteron in, 31
embryos, 23
fossil, 515

Rana aesopus, 97
Rana arvalis, hybridization in, 41
Rana aurora draytonii, 420
Rana boylii boylii, 66, 392
Rana burnsi, 87

Rana catesbeiana, 98, 120, 190, 292,

381, 444, 454, 457
Rana cavity mpanum, 334
Rana christyi, 517

Rana clamitans, 120, 141, 332, 342,
344, 345, 395, 396, 405, 435,
454, 487

Rana esculenta, 88, 109, 144, 275,

411, 432, 436
Ranafusca, 115, 420

hybridization in, 41
Rana grayi, 442
Rana heckscheri, 137
Rana hexadactyla, 244, 433
Rana holstii, 118
Rana kandiyohi, 87
Rana mascareniensis, 510, 517
Rana ornatissima, 416
Rana palustris, 135, 457

somatic number of chromosomes,
18

Rana pipiens, 18, 80, 87, 145, 146,
152, 183, 271, 281, 293, 299,
310, 344, 345, 392, 419-421,
433, 454, 457

Rana septentrionalis, 137

Rana sphenocephala, 407

Rana spinosa7 110

Rana sylvatica, 18, 112, 113, 152,
276, 277, 345, 410, 445

Rana temporaria, 85, 113, 181, 183,
268, 270, 277, 393, 434

Rana virgatipes, 97, 408

Ranaster, 497

Ranavus, 515

Ranidae, 64, 237, 449, 505, 515-524,
527

Raninae, 518, 520
Ranodon, 49, 242
Ranodon sibiricus, 467
Rappia, 525
Rasping organs, 139
Razwilowska, 393

570

THE BIOLOGY OF THE AMPHIBIA

Reaction, defense fight, 383

feeding, 383

time to light, 419
Receptors, 317

heat and cold, 322
Recta, 88

Rectus abdominis, 248, 254
Rectus internus, 333
Reed, 222, 335
Reed and Kingsbury, 222
Reese, 421

Reflex arcs, 354, 377
Reflexes, in Ambystoma, develop-
ment of, 378

multiple uses of, 380

preservation, 391

snapping, 384

swimming, 382

"unken," 380

of walking, 379, 382
Refractory period, 194
Regeneration, 36-37

capacity, 39-40
Regenerative territories, 40
Reis, 104, 149
Reiter and Zondeck, 295
Relationships and classification, 469-
543

Renal corpuscle, 268, 273
Renal portal system, 186
Rennin, 206
Rensch, 80

Reproductive system, 266, 272
Resonating organs, 408
Resonating sacs, 170
Respiration, 13, 186, 208
buccopharyngeal, 166, 171, 172,
192

cutaneous, 166, 171, 186, 192

integument in, 163

pulmonary, 171

ways of, 170
Respiratory mechanism, 174
Respiratory organs, larval, 61
Respiratory responses, 175
Respiratory system, 158-178
Respiratory structures, 65
Respiratory tail, 73

Response, geotropic, 401

to humidity change, 421

to internal stimulation, 347

phototropic, 401

respiratory, 175

stereotropic, 418

to temperature change, 418
Rete cords, 277
Reticular formation, 365, 369
Retina, 34, 145, 151, 330, 331

rods and cones of, 93
Retractor bulbi, 333
Retractor tentaculi, 333
Rhacophorus, 66
Rheotropism, 346
Rhinatrema, 76, 465
Rhinesuchidae, 460
Rhinoderma, 71, 74, 415, 507
Rhinodermatinae, 606, 507
Rhinophryninae, 500, 501
Rhinophrynus, 79, 140, 500, 501,
503

Rhizopoda, 440
Rhombophryne, 530
Rhombophryninae, 529-531
Rhyacotriton, 51, 167, 260, 262,

285, 472, 473
Rhynophrynus dorsalis, 501
Ribbing, 259
Ribs, 11, 229, 232, 244

abdominal, 234

sacral, 7
Ridewood, 226
Ridewood and Howes, 243
Riech, 310
Riley, 345, 418
Risser, 340

Ritter and Miller, 173
Robson, 80, 84
Rods, 330
RogofT, 388

Rohon-Beard cells, 370
Rollinat, 42
Romeis, 293

Romer, 9, 10, 255, 459, 462
Rose, 66, 69, 115
Rothig, 357, 358, 362, 367
Rubner, 432, 434
Ruud, 33

INDEX

571

Ruzicka, 140
Rylkoff, 256

Sacculus, 335
Sacral ribs, 240
Sacrum, 231, 244

variations in, 239
St. Hiller, 210

Salamander, 148, 166, 168, 175, 176,

187, 190, 192, 253, 257, 259, 260
Salamandra, 53, 54, 109, 134, 252,

328, 331, 387, 401, 402, 419,

436, 473, 474, 476, 477
Salamandra atra, 53, 54, 59, 94, 135,

168, 282, 320, 388
Salamandra caucasica, 118, 388, 389
Salamandra luschani, 118
Salamandra salamandra, 53, 54, 94,

97, 134, 135, 137, 143, 146, 149,

150, 321, 388, 421, 476
Salamandrella, 46, 91
Salamandridae, 52, 55, 146, 167,

389, 472, 473-476
Salamandrina, 91, 167, 168, 173,

388, 416, 454, 475
Salamandrina terdigitata, 47 '6
Salamandroidea, 465, 471, 473
Sailer, 110
Salts, 205
Samandaridin, 134
Samandarin, 134
Samandatrin, 135
Sanders, 440
Saprolegnia, 438
Sarasin, 132
Sartorius, 260
Sasaki, 386
Saurabatrachia, 465
Sayle, 321, 341, 421
Scales, 1, 8, 130, 158
modern and extinct, 8
placoid, 219
Scaphiophryne, 529
Scaphiopus, 97, 119, 140, 218, 406,

444, 493, 494

Scaphiopus hammondi, 403, 406,

408, 415, 421
Scaphiopus holbrookii, 406, 407, 409,

494
Scapula, 234
Scapulo-coracoid, 234
Schaeffer, 393
Schaxel, 39
Scheminsky, 340
Schlampp, 333
Schlosser, 388
Schmalhausen, 33, 49, 242
Schmid, 367
Schmidt, 141, 144
Schnakenbeck, 144
Schotte, 28, 40
Schoutedenella, 515
Schoutedenella globosa, 516
Schrader, 360, 363, 366
Schreitmuller, 40, 388
Schultz, 194

Schulze and Holldobler, 310
Sclera, 327
Scotobleps, 517, 518
Scott, 438

Scott, Biraben, and Fernandez-

Marcinowski, 66
Scutes dermal, 520
Scutiger, 433, 492, 493
Secondary sex characters, 108, 114,

116, 117, 119, 121, 123, 305
Segmentation of gonads, 280
Selection, natural, 86
Sembrat, 293, 296
Semicircular canals, 336
Semimembranosus, 260, 262
Seminiferous tubules, 277
Semitendinosus, 260
Sense, olfactory, 412
Sense organs and their functions,

317-352
Senses, dominant, 340
Sensitivity to light, vision and, 343
Septomaxillary, 215
Serratus, 257
Severinghaus, 30
Sewertzoff, 101
Sex, chromosome, 121
cry, 409

572

THE BIOLOGY OF THE AMPHIBIA

Sex defined, 108

differences in skull, secondary, 123
identification of, 285
and its modification, 276
products, 299
recognition of, 115, 410
by color, 412
skin glands, 412
reversal, 278

and secondary sex characters,
108-129
Sexual activity, 180, 394
Sexual characters, secondary, 116,

117, 119, 305
Sexual differences, in color, 116

unexplained, 112
Sexual dimorphism, 121

of forelimbs, 110
Sexual modification of manus, sec-
ondary, 114
Seydel, 325

Shelford, 84, 400, 419, 421
Shipley and Wislocki, 135
Shoulder and arm musculature, 266
Shoulder girdle, 12, 33
Simomantis, 524
Sinus venosus, 189, 194
Siren, 50, 97, 102, 103, 134, 138
161, 192, 203, 215, 233, 236,
240, 280, 293, 294, 325, 326,
357, 358, 367, 410, 416, 436,
443, 463, 484, 485
Siren lacertina, heart of, 193
Sirenidae, 48, 50, 52, 283, 484, 485
Skeleton, 212-246, 248

of early Amphibia, 212

laryngeal, 226

of modern Amphibia, 244

in phylogenetic studies, 29

visceral, 222
Skin, 12, 103, 130, 133, 145, 162

capillaries, 163

as respiratory organ, 4, 140

rugositj^, 90

shedding, 139

texture, 96, 127

transplanting, 149

Skull, 12, 30, 212, 244

bones, 102

of Embolomeri, 212

evolution of, 214

progressive modification of, 213
Skuse, 441
Sluiter, 147
Small intestine, 204
Smell, 340
Sminthillus, 70, 506
Smith, 48, 145, 180, 225, 264, 281,

296, 298-300, 386
Smith and Smith, 298
Smooth muscle, 301
Snyder, 370
Soderberg, 358, 367
Sollas, 11, 463
Somites, 31, 214
Sooglossinae, 492, 494, 495
Sooglossus, 494, 495
Sooglossus gardineri, 494, 495
Sooglossus sechellensis, 494, 495
Sound stimulus, 342
Sound transmitting apparatus, 334
Spade, 242

Spade-foot Toad, 493, 494
Spaul, 299, 301
Spaul and Howes, 299
Spawning, 180

Speciation, and adaptation, 79-108

by dwarfing, 99

in Plethodon, 456
Species, defined, 80

and subspecies, 42
Speidel, 309
Spelaeophryne, 539
Spelerpes, 483
Spemann, 21, 26, 27, 32
Sped er pes f use us, 483
Sperm, 101

Spermatheca, 16, 40, 283

evolution of, 285
Spermatic ampullae, 273
Spermatogenesis, 18, 280, 307
Spermatophores, 17, 109, 115, 283,
387

Spermatozoa, 15, 16, 40, 74, 108,
273

INDEX

573

Sphenethmoid, 215

Sphenophryne, 531, 532

Sphenophryninae, 531, 532

Spinal cord, 196, 354, 365

Spinal ganglia, 370

Spiracles, 24, 62, 71, 159, 166

Spiracular notch, 6

Spiral valve, 187

Spleen, 180, 184

Splenials, 213

Sporozoa, 440

Spring Peeper, 72

Springer, 140, 436

Squamosal, 215, 264

Stapedial artery, 222

Stapedial muscle, 222

Stapes, 6, 221, 223

Staurois, 64, 138, 521-524

Steen, 272

Stegopidae, 462

Stegops, 10

Steiner, 241, 366

Steinitz, 34

Steinmann, 346

Stereochilus, 318, 390, 480

Stereocyclops, 536

Stereospondyli, 8, 213, 229, 234,

459, 460, 461
Stereotropic response, 418
Sterility, 88
Sternohyoideus, 254
Sternum, 233, 237
Stewart, 175
Stier, 345
Stockard, 147
Stohler, 18

Stomach, 151, 202, 204, 206

glands, 204
Stone, 30

Storer, 62, 97, 112, 115, 133, 388,
400, 403, 405, 408, 414-416,
444, 454

Stratum corneum, 102

Streeter, 335, 339

Streuli, 330

Striated muscle, 247

Striatum, 358

Strotgen, 388
Stumpffia, 529, 531, 539
Stutzer, 438
Subba Rau, 192
Subclavian vein, 195
Subcoracoscapularis, 259
Subintestinal vessel, 185, 187
Sublingual tonsil, 184
Subpallium, 358

Suctorial disc of mountain-brook

tadpole, 65
Sugars, 207
Sulze and Garten, 433
Sumi, 298

Superior labial cartilage, 24
Superior olive, 365
Supernumerary limbs, 40
Supracleithrum, 234
Supracoracoideus, 258
Supraoccipital, 214
Suprarostral cartilage, 62
Suprascapula, 222
Surface, 415

Surface law of energy consumption,

434
Survival, 84
Sushkin, 222
Sweet, 269
Swett, 33, 38, 39
Swimming reflex, 382
Swingle, 145, 294, 295, 300, 304
Sympathetic ganglion, 370, 373
Sympathetic impulses, 248
Sympathetic outflow, 371
Sympathetic trunks, 373
Symphygnathinae, 534-536
Symphysial bones, 221
Symplectic, 221
Synangial valves, 190
Synangium, 189, 191
Synapse, 353
Syngamy, 17
Syrrhophus, 70, 500, 506
Systemic arch, 187
Systolic pressure, 193
Szab6, 443
Szymanski, 347, 419

574

THE BIOLOGY OF THE AMPHIBIA

Tabular, 9, 221
Tactile organs, 321
Tadpoles, 74, 171, 195, 209

carried on back of male parent,
60, 70

mouths, 63

regeneration of gills in, 36
snout of, 121
Tago, 399

Tail, fin, 57, 61, 145

loss of, 187

musculature, 249

prehensile, 114, 253

regeneration of, 36, 39
Tails, 12, 56, 58, 73, 102-104, 113,

132, 187, 208
Tait and McNally, 338
Taniguchi, 150
Tarsalia, 33, 242, 243
Taste, 340

bud, 202, 322

organs of, 322
Taylor, 85

Tectorial membrane, 337
Teeth, 8, 9, 92, 102, 104, 123, 124,
125, 139

effect of testicular hormone on,

306
egg, 73

epidermal, 102
in frog tadpoles, 24
labyrinthodont, 213
larval, 139
loss of, 91

of male Hydromantes platycephalus
elongated, 125

maxillary, 124, 126
Telencephalon, 357
Telmatobius, 499
Telmatobius jelskii, 117
Temperature, 86, 98, 193, 194

and behavior, 433

body, 431

change, responses to, 418
optimum, 421, 435
preferences, 420
Temporal and back muscles, 12

Temporal bones, 12
Temporal muscles, 215
Temporalis, 251, 263, 264
Ten Cate, 370, 391
Tendons, 110
Tensor chorioideae, 330
Tensor fasciae latae, 262
Terrestrial Plethodontids, 57
Testes, 109, 273, 275
Testicular hormone, 307
Tetrapods, 174

first, 2, 256

skull early, 212
Tetraprion, 512
Thalamencephalon, 357
Thalamofrontal tract, 362
Thalamus, 358, 360, 367, 369
Thigmotaxis, 346

Throat, ventral musculature, 249,
254

Thrombocyte, 179, 182, 184
Thumb, 126, 135, 139, 241
Thymus, 292, 308, 309
Thyroid, gland, 35, 98, 226, 291-
292

hormone, 98, 102, 103, 140, 296

and metamorphosis, 292-295

processes, 170
Thyroidectomy, 140

effect of, on regeneration, 39
Tibia, 243

Tibiale, 33, 242, 243
Tilney and Warren, 309
Toads, aglossal, 489

burrowing, 96

faces, 96

fossil, 495, 504

narrow-mouthed, 527

Pelobatid, 493

Pipid, 490

Spade-foot, 493
Toes, 62, 111, 114

loss of, 91, 92, 97

of tree frog friction pad, 135

webs, 113
Tongue, 201

boletoid, 202

form, 90, 201

grooved, 533

INDEX

575

Tongue, muscles, 226, 254
Tonic immobility, 424, 425
Tonsils, 184
Tooth form, 127

Tooth patches, parasphenoid, 122
Tooth rows, 65-68, 74-76
Torelle, 344, 418
Tornier, 151

Torreblanca, Benjamin, and Allen,
299

Trabecula, 29, 30

Trachea, 168-170

Tracheal lung, 166

Transplanting tissues during gas-

trulation, 26
Transverse process, 9, 11, 229
Trematoda, 441
Trematops, 242, 243
Trematopsidae, 460
Trematosauridae, 461
Tretjakoff, 330
Triceps, 259
Trimerorachidae, 460
Triplicate formation, 39
Triprion, 130, 512
Triprion petasatus, 513
Triturus, 41, 52, 309, 328, 343, 474-

476

hybridization in, 42
Triturus alpestris, 151, 214
Triturus cristatus, 115, 143, 475

hybridization in, 42
Triturus dorsalis, 475
Triturus meridionalis, 475
Triturus palmatus, 113
Triturus pyrrhogaster, 111, 112, 114,

115, 150, 387, 388, 443
Triturus torosus, 52, 112, 388, 475
Triturus viridescens, 52, 53, 109,

388, 438, 444, 475
Triturus vittatus, 115
Trochlear, 361
Tropistic response, 344
Truncus, 191
Trypanosoma, 438, 439
Trypsin, 206, 207
Tsusaki and Okajima, 327
Tubercle, 138, 172, 233
Twinning, 40

Twitty, 29, 131

Tylototriton, 52, 132, 218, 233,

387, 449, 474-476
Tympanic annulus, 35, 222
Tympanum, 31, 35, 221, 226, 333
Typhlomolge, 104, 285, 294, 333,

480

Typhlonectes, 76, 141, 166, 320, 465
Typhlotriton, 92, 97, 98, 149, 150,
333, 346, 347, 421, 480
effect of light on, 34
Tyrosin, 148, 150

Ubisch, 39
Ueki, 111

Uhlenhuth, 35, 291, 293, 298
Uhlenhuth and Schwartzbach, 298
Ulna, 241
Ulnare, 242

Ultimobranchial body, 166, 308
Umbrella mouth, 69, 70
Unicellular glands, 131
Unken reflex, 380, 381
Urea, 207, 208, 266
Ureters, 272, 275
Uric acid, 266
Urinary bladder, 23, 276
Urine concentration, 271
Urogenital system, 5, 266-289

stages, in transformation, 279
Urostyle, 230
Uterus, 74

bicornuate, 273
Utricular macula, 336, 339
Utriculus, 335

Vagus, 176, 193, 263, 366, 367
Vallois, 257
Valves, 186, 195

paradox, 192

semilunar, 189

spiral, 191, 192
Vandel, 393
Van der Heyde, 436

THE BIOLOGY OF THE AMPHIBIA

576

Van Leeuwen, 109

Van Nifterik, 342

Van Nifterik and Bruyn, 390

Van Rynberk, 370

van Seters, 222

Van't Hoff's law, 431

Variation, 80

Vasa efferentia, 273, 275, 277
Vascular system, 179

development of, 185

of Necturus maculosus, 188
Vascular villosities, 110
Vasoconstrictors, 194
Vasomotor system, 175
Vavilov, 88
Vein, cardinal, 185

ischiadic, 196
Vena cava, 186

posterior, 186
Ventricle, 189, 190, 192, 194
Verrier, 328
Versluys, 252

Vertebrae, 8, 9, 10, 226, 227, 250, 605

coccygeal, 231

development of, 230

of extinct Amphibia, 228

opisthocoelous, 229

presacral, 231

procoelous, 229
Vertebral columns of Salientia, 488
Vertebral veins, 196
Verworn, 381
Vesicula seminalis, 276
Vestibular nucleus, 365
Vialli, 309, 310
Vidal, 495
Vincent, 304
Viscera, 111, 151
Visceral arches, 166, 223
Visceral muscles, 263
Visceral skeleton, 222
Visher, 455

Vision and sensitivity to light, 343
Visual cells, 332
Vitelline mass, 205
Vitelline membrane, 19, 281
Vitreous humor, 331
Vocal cords, 169, 170

Vocal organs, 170

Vocal pouch, 71, 109, 120, 400

Vocal sac, 170, 408

external, 408

internal, 408
Vogt, 21

Voice, 87, 110, 406

clue to species, 407

recognition of sex, 408

significance of, 408
von Baer, 101
von Braunmuhl, 184
Vorticella, 439
Voss, 282

Wager, 64, 66, 67
Waggener, 308
Walker, 270

Walking, reflexes of, 379, 382
Wallace, 426
Walter, 40

Warren and Tilney, 309
Wastl and Seliskar, 159
Water dog, 112

Watson, 3, 5, 6, 213, 221, 223, 239,
241, 243, 459, 460, 462

Ways of Amphibia, 399-430

Webbing, 99, 113

Weber, 16, 205, 281

Weed, 87

Weiss, 37, 194

Wellman, 406

Welti, 305

Wenrich, 439

Wenyon, 438

Werner, 93, 146, 147, 151

Werneria, 501, 502

Wertheimer, 341

Westphal, 36

Wetzel, 282

Whipple, 240

Whiteside, 337

Whitman, 345, 391, 413

Whittard, 461, 462

Wilder, 102, 132, 136, 138, 140,
256, 292, 308, 323, 325, 346.
413

N -

INDEX 577

Willem, 173
Williston, 3
Wintrebert, 5, 16, 131
Witschi, 85, 277
Wolf, 299

Wolffian duct, 269, 272, 273, 276
WolterstorfT, 40, 150, 419, 443
Wood Frog, 143
Worm Salamander, 482
Woronzowa, 151

Wright, 62, 135, 322, 387, 399, 419,

442, 456
Wright and Allen, 386
Wright and Wright, 74
Wunderer, 53
Wurmbach, 36

Xenobatrachus, 535, 538
Xenobatrachus bidens, 535
Xenobatrachus giganteus, 535
Xenobatrachus macrops, 535
Xenobatrachus rostratus, 535
Xenopinae, 489

Xenopus, 131, 145, 164, 172, 215,
216, 231, 321, 400, 418, 461,
489, 490, 491, 496

Xenopus clivii, 490

Xenopus laevis, 490

Xenorhina, 535

X-rays, 85

Yamagiva, 273, 274
Yerkes, 342, 390, 395, 396, 405
Yosemite Salamander, 483
Ypsiloid apparatus, 477
Yung, 111, 209

Zachaenus, 327, 500
Zatrachydae, 460
Zeleny, 40
Zelleriella, 440
Zenneck, 147
Zepp, 110, 112
Zona pellucida, 281
Zona radiata, 281
Zondeck and Reiter, 295

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